United States

Department

of Agriculture

Forest Service

Rocky Mountain

Research Station

Proceedings

RMRS-P-21

September 2001

Shrubland Ecosystem

Genetics and Biodiversity:

Proceedings
Rocky Mountain Research Station

324 25th Street

Ogden, UT 84401

Abstract

McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland ecosystem genetics and biodiversity: proceedings; 2000

June 13–15; Provo, UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research

Station. 365 p.

The 53 papers in this proceedings include a section celebrating the 25-year anniversary of the Shrub Sciences Laboratory

(4 papers), three sections devoted to themes, genetics, and biodiversity (12 papers), disturbance ecology and biodiversity

(14 papers), ecophysiology (13 papers), community ecology (9 papers), and field trip section (1 paper). The anniversary session papers

emphasized the productivity and history of the Shrub Sciences Laboratory, 100 years of genetics, plant materials development for

wildland shrub ecosystems, and current challenges in management and research in wildland shrub ecosystems. The papers in each

of the thematic science sessions were centered on wildland shrub ecosystems. The field trip featured the genetics and ecology of

chenopod shrublands of east-central Utah. The papers were presented at the 11th Wildland Shrub Symposium: Shrubland Ecosystem

Genetics and Biodiversity held at the Brigham Young University Conference Center, Provo, UT, June 13–15, 2000.

Keywords: wildland shrubs, genetics, biodiversity, disturbance, ecophysiology, community ecology

The use of trade or firm names in this publication is for reader information and does not imply

endorsement by the U.S. Department of Agriculture or any product or service

Acknowledgments

We thank the many people and organizations that assisted in the advance preparation and conduct of the symposium, anniversary

celebration, and field trip. Brigham Young University President Merrill J. Bateman, Rocky Mountain Research Station Director Denver

P. Burns, and Forest Service Vegetation Management and Protection Washington Office Director William T. Sommers kindly helped

with the anniversary celebration. Members of the A. Perry Plummer and Howard C. Stutz families including Mrs. Blanch Plummer

and Dr. Howard and Mrs. Mildred Stuz were present at the bust unveiling, which honored the contributions of Mr. Plummer and Dr.

Stutz in establishment of the Shrub Sciences Laboratory. Stacia Simonsen, Von Phillips, and Rob Holcombe and other staff members

of the Brigham Young University Conferences and Workshop staff were gracious, accommodating, and efficient in all aspects of the

symposium and field trip preparation and conduct. Pat Ford, Geneva Ball, Stewart Sanderson, and Stan Kitchen of the Shrub

Sciences Laboratory, Gary Jorgensen of the Great Basin Experimental Range, and volunteer Roberta Leslie helped with logistical

and clerical support. Technical sessions were chaired by Durant McArthur, Kent Ostler, Scott Walker, Darrell Ueckert, Ann Hild, and

Bruce Roundy. Daniel Fairbanks sculpted the busts and assisted the Plummer and Stutz families with the bust unveiling. Marcus

Alan Vincent prepared the cover illustration with its five shrub species (black greasewood, big sagebrush, fourwing saltbush, rubber

rabbitbrush, and Stansbury cliffrose). Several units of the Shrub Research Consortium made financial contributions to assist with

proceedings publication costs including the Shrub Sciences Laboratory, Brigham Young University College of Biology and

Agriculture and Department of Botany and Range Science, Utah State University, Utah Division of Wildlife Resources, University

of Idaho, Montana State University, University of Nevada-Reno, Texas A&M System-Texas Agricultural Experiment Station, Texas

Tech University, Washington State University, University of Wyoming, U.S. Department of Agriculture Agricultural Research ServiceJornada Experimental Range, Batelle Pacific Northwest Laboratories, and Bechtel Nevada. We thank the Rocky Mountain Research

Station Publishing Service Unit for preparing the final publication.

E. Durant McArthur

Daniel J. Fairbands

Compilers

Publisher’s note: Papers in this report were reviewed by the compilers. Rocky Mountain Research

Station Publishing Services reviewed papers for format and style. Authors are responsible for content.
Compilers

E. Durant McArthur, Project Leader, U.S. Department of Agriculture, Forest Service, Rocky

Mountain Research Station, Shrub Sciences Laboratory, Provo, UT

Daniel J. Fairbanks, Professor, College of Biology and Agriculture, Department of Botany and

Range Science, Brigham Young University, Provo, UT

Shrubland Ecosystem Genetics and

Biodiversity: Proceedings

Provo, UT, June 13–15, 2000
Shrub Research Consortium

USDA Forest Service, Rocky Mountain Research Station, Shrub Sciences Laboratory*, Provo, Utah,

E. Durant McArthur (chair)

Brigham Young University*, Provo, Utah, Daniel J. Fairbanks

USDA Agricultural Research Service, Renewable Resource Center*, Reno, Nevada, James A. Young

Utah State University*, Logan, Eugene W. Schupp

State of Utah, Department of Natural Resources, Division of Wildlife Resources*, Ephraim, Scott C. Walker

University of California, Los Angeles, Philip W. Rundel

Colorado State University, Fort Collins, William K. Lauenroth

University of Idaho, Moscow, Steven J. Brunsfeld

University of Montana, Missoula, Donald J. Bedunah

Montana State University, Bozeman, Carl L. Wambolt

University of Nevada, Reno, Paul T. Tueller

University of Nevada, Las Vegas, Stanley D. Smith

Oregon State University, Corvallis, Lee E. Eddleman

New Mexico State University, Las Cruces, Kelly W. Allred

Texas A & M System, Texas Agricultural Experiment Station, San Angelo, Darrell N. Ueckert

Texas Tech University, Lubbock, Ronald E. Sosebee

USDA Agricultural Research Service, High Plains Grassland Research Station, Cheyenne, Wyoming,

D. Terrance Booth

USDA Agricultural Research Service, Jornada Experimental Range, Las Cruces, New Mexico, Jerry R. Barrow

USDA Forest Service, Rocky Mountain Research Service, Great Basin Ecology Laboratory, Reno, Nevada,

Robin J. Tausch

University of Utah, Salt Lake City, James R. Ehleringer

Weber State University, Ogden, Utah, Barbara A. Wachocki

Washington State University, Pullman, Benjamin A. Zamora

University of Wyoming, Laramie, Stephen E. Williams

Battelle Pacific Northwest Laboratories, Richland, Washington, Janelle L. Downs

Bechtel Nevada, Las Vegas, Nevada, W. Kent Ostler

*Charter members

The Shrub Research Consortium was formed in 1983 with five charter members (see list). Over time SRC has grown to its present

size of 25 institutional members. The SRC had three principal objectives in its charter: (1) developing plant materials for shrubland

rehabilitation; (2) developing methods of establishing, renewing, and managing shrublands in natural settings; and (3) assisting with

publication and dissemination of research results. These objectives have been met by a series of symposia sponsored by the

Consortium and partners. This publication is the 11th in the series; the previous 10 are listed on the next page. Proceedings of all

publications to date have been published by the U.S. Department of Agriculture, Forest Service, Intermountain Research Station and

Rocky Mountain Research Station. The executive committee has plans for additional symposia. The next one will be held in Laramie,

WY, in 2002 with a shrubland ecosystem seeds and soil theme. Each symposium has had a theme, but the executive committee

has encouraged attendance and participation by shrubland ecosystem biologists and managers with wider interests than any particular

symposium theme—the heart of the Consortium’s programs are wildland shrub ecosystem biology, research, and management.

ii
Availability of Previous Wildland Shrub Symposia Proceedings

First: Tiedemann, A. R.; Johnson, K. L., compilers. 1983. Proceedings—research and management of bitterbrush and cliffrose

in Western North America; 1982 April 13–15; Salt Lake City, UT. General Technical Report INT-152. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station. 279 p. Out of print—

available from National Technical Information Service as document PB83-261537 A13.

Second: Tiedemann, A. R.; McArthur, E. D.; Stutz, H. C.; Stevens, R.; Johnson, K. L., compilers. 1984. Proceedings—symposium

on the biology of Atriplex and related chenopods; 1983 May 2–6; Provo, UT. General Technical Report INT-172. Ogden,

UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station. 309 p. Out

of print—available from National Technical Information Service as document PB85-116358 A14.

Third: McArthur, E. D.; Welch, B. L., compilers. 1986. Proceedings—symposium on the biology and management of Artemisia

and Chrysothamnus; 1984 July 9–13; Provo, UT. General Technical Report INT-200. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Research Station. 398 p. Out of print—available from National Technical

Information Service as document PB86-182318 A18.

Fourth: Provenza, F. D.; Flinders, J. T.; McArthur, E. D., compilers. 1987. Proceedings—symposium on plant herbivore

interactions; 1985 August 7–9; Snowbird, UT. General Technical Report INT-222. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Research Station. 179 p. A few copies are available from the Rocky Mountain

Research Station; otherwise available from National Technical Information Service as document PB90-228578 A09.

Fifth: Wallace, A.; McArthur, E. D.; Haferkamp, M. R., compilers. 1989. Proceedings—symposium on shrub ecophysiology

and biotechnology; 1987 June 30–July 2; Logan, UT. General Technical Report INT-256. Ogden, UT: U.S. Department

of Agriculture, Forest Service, Intermountain Research Station. 183 p. Available from the Rocky Mountain Research

Station.

Sixth: McArthur, E. D.; Romney, E. M.; Smith S. D.; Tueller, P. T., compilers. 1990. Proceedings—symposium on cheatgrass

invasion, shrub die-off, and other aspects of shrub biology and management; 1989 April 5–7; Las Vegas, NV. General

Technical Report INT-276. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station.

351 p. Out of print—available from National Technical Information Service as document PB91-117275 A16.

Seventh: Clary, W. P.; McArthur, E. D.; Bedunah, D.; Wambolt, C. L., compilers. 1992. Proceedings—symposium on ecology and

management of riparian shrub communities; 1991 May 29–31; Sun Valley, ID. General Technical Report INT-289.

Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station. 232 p. Out of print—

available from National Technical Information Service as document PB92-227784 A11.

.

Eighth: Roundy, B. A.; McArthur, E. D.; Haley, J. S.; Mann, D. K., compilers. 1995. Proceedings: wildland shrub and arid land

restoration symposium; 1993 October 19–21; Las Vegas, NV. General Technical Report INT-GTR-315. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Research Station. 384 p. Available from the Rocky Mountain

Research Station.

Ninth: Barrow, J. R.; McArthur, E. D.; Sosebee, R. E.; Tausch, R. J., compilers. 1996. Proceedings: shrubland ecosystem

dynamics in a changing environment; 1995 May 23–25; Las Cruces, NM. General Technical Report INT-GTR-338.

Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station. 275 p. Available from the

Rocky Mountain Research Station.

Tenth: McArthur, E. D.; Ostler, W. K.; Wambolt, C. L., compilers. 1999. Proceedings: shrubland ecosystem ecotones; 1998

August 12–14; Ephraim, UT. Proceedings RMRS-P-11. Ogden, UT: U.S. Department of Agriculture, Forest Service,

Rocky Mountain Research Station. 299 p. Available from the Rocky Mountain Research Station.

iii

Contents

page

Anniversary Celebration .....................................................................................................................................1

E. Durant McArthur The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective ...........3

Daniel J. Fairbanks A Century of Genetics ..............................................................................................42

Stephen B. Monsen Development and Use of Plant Resources for Western Wildlands ..........................47

Nancy L. Shaw

William T. Sommers Scientific Challenges in Shrubland Ecosystems.......................................................62

Genetics and Biodiversity.................................................................................................................................65

Joan Vallès Artemisia Systematics and Phylogeny: Cytogenetic and .........................................67

E. Durant McArthur Molecular Insights

Stewart C. Sanderson Chromosome Races of Fourwing Saltbush (Atriplex canescens), ...........................75

Howard C. Stutz Chenopodiaceae

Brian D. Vanden Heuvel A Molecular Phylogeny for Cercocarpus H.B.K. (Rosaceae) Using the

C. Randal Linder External Transcribed Spacer of the Nuclear Ribosomal Repeat ..............................89

Alisa P. Ramakrishnan Microsatellite Markers and Polymorphism in Cheatgrass.........................................95

Craig E. Coleman (Bromus tectorum L.)

Susan E. Meyer

Daniel J. Fairbanks

Lyuba A. Kapustina Biodiversity, Ecology, and Microelement Composition of Kyzylkum

Desert Shrubs (Uzbekistan) .....................................................................................98

Lyubov A. Kapustina Artemisia Communities in Arid Zones of Uzbekistan (Central Asia).......................104

Montserrat Torrell

Joan Vallès

Blair L. Waldron Kochia prostrata Germplasm Collection Expedition to Kazakhstan .......................113

R. Deane Harrison

Nicolai I. Dzyubenko

Auskhan Khusainov

Sergey Shuvalov

Sergey Alexanian

John H. Graham Narrow Hybrid Zone Between Two Subspecies of Big Sagebrush

E. Durant McArthur (Artemisia tridentata: Asteraceae): XI. Plant-Insect Interactions in

D. Carl Freeman Reciprocal Transplant Gardens ..............................................................................118

D. Carl Freeman Use of Distance Measures to Assess Environmental and Genetic

John H. Graham Variability Across Sagebrush Hybrid Zones ...........................................................127

Terra Jones

Han Wang

Kathleen J. Miglia

E. Durant McArthur

Andrés F. Cibils Phenotypic Sex Ratios of Atriplex canescens Shrubs in Relation to

David M. Swift Cattle Browsing ......................................................................................................134

Richard H. Hart

v
Simon A. Lei Ecological and Population Genetics of Locally Rare Plants: A Review ..................139

L. St. John New Plant Releases From the USDA-NRCS Aberdeen, Idaho, Plant

P. Blaker Materials Center .....................................................................................................143

Disturbance Ecology and Biodiversity ........................................................................................................145

Jayne Belnap What Makes the Desert Bloom? Contribution of Dust and Crusts

Richard Reynolds to Soil Fertility on the Colorado Plateau .................................................................147

Marith Reheis

Susan L. Phillips

Mark Miller Components of Spatial and Temporal Soil Variation at Canyonlands

Jayne Belnap National Park: Implications for P Dynamics and Cheatgrass

Susan Beatty (Bromus tectorum) Performance ............................................................................154

Bruce Webb

Angela D. Yu Equilibrium Theory of Island Biogeography: A Review...........................................163

Simon A. Lei

Simon A. Lei Vegetation Response to Natural and Anthropogenic Disturbances in

the Larrea-Ambrosia and Coleogyne Shrublands ..................................................172

Jeffrey E. Ott Plant Community Dynamics of Burned and Unburned Sagebrush and

E. Durant McArthur Pinyon-Juniper Vegetation in West-Central Utah ...................................................177

Stewart C. Sanderson

Jason L. Vernon Response of Residual Native Species After Two-Way Chaining and

Val Jo Anderson Seeding in Utah ......................................................................................................192

James N. Davis

Stanley G. Kitchen Winterfat Decline and Halogeton Spread in the Great Basin .................................200

Gary L. Jorgensen

Robin E. Durham Predicting First-Year Bare-Root Seedling Establishment With Soil and

Benjamin A. Zamora Community Dominance Factors .............................................................................204

Michael R. Sackschewsky

Jason C. Ritter

Blair L. Waldron Forage Kochia: Friend or Foe.................................................................................210

R. Deane Harrison

N. Jerry Chatterton

Burke W. Davenport

Barbara A. Wachocki Impact of Tebuthiuron on Biodiversity of High Elevation Mountain Big

Mohammad Sondossi Sagebrush Communities ........................................................................................216

Stewart C. Sanderson

Bruce L. Webb

E. Durant McArthur

Susan E. Meyer Factors Mediating Cheatgrass Invasion of Intact Salt Desert Shrubland ...............224

Susan C. Garvin

Julie Beckstead

Lance T. Vermeire Sand Sagebrush Response to Fall and Spring Prescribed Burns ..........................233

Robert B. Mitchell

Samuel D. Fuhlendorf

Russell Fox Managing Saltcedar After a Summer Wildfire in the Texas Rolling Plains .............236

Rob Mitchell

Mike Davin

vi
W. K. Ostler Biodiversity Analysis of Vegetation on the Nevada Test Site .................................238

D. J. Hansen 

Ecophysiology ...................................................................................................................................................249

R. S. Criddle Determination of Plant Growth Rate and Growth Temperature Range

B. N. Smith From Measurement of Physiological Parameters...................................................251

L. D. Hansen

J. N. Church

Lee D. Hansen Responses of Plant Growth and Metabolism to Environmental Variables

Bruce N. Smith Predicted From Laboratory Measurements ............................................................259

Richard S. Criddle

J. N. Church

Lyneen C. Harris Effects of Salinity and Temperature on Respiratory Metabolism of

M. Ajmal Khan Salicornia utahensis From a Great Basin Playa .....................................................265

Jiping Zou

Bruce N. Smith

Lee D. Hansen

V. Wallace McCarlie Respiratory and Physiological Characteristics in Subpopulations

Lee D. Hansen of Great Basin Cheatgrass .....................................................................................271

Bruce N. Smith

Bruce N. Smith Temperature-Dependent Respiration-Growth Relations in Ancestral

Jillian L. Walker Maize Cultivars .......................................................................................................276

Rebekka L. Stone

Angela R. Jones

Lee D. Hansen

Dorothy A. Stradling Calorimetric Studies of Cryptogamic Crust Metabolism in Response to

Tonya Thygerson Temperature, Water Vapor, and Liquid Water........................................................280

Bruce N. Smith

Lee D. Hansen

Richard S. Criddle

Rosemary L. Pendleton

Tonya Thygerson Microcalorimetric Studies on Metabolic and Germination Response to

D. Terrance Booth Temperature for Three Populations of Winterfat (Eurotia lanata)...........................283

Jennifer M. Harris

Lee D. Hansen

Bruce N. Smith

D. J. Weber Composition of Vegetable Oil From Seeds of Native Halophytes ..........................287

B. Gul

A. Khan

T. Williams

N. Williams

P. Wayman

S. Warner

Jerry R. Barrow Carbon Transport by Symbiotic Fungi in Fourwing Saltbush,

Atriplex canescens (Pursh) Nutt. ............................................................................291

Lee Walls Nitrogen-Fixing Nodule Characterization and Morphology of Four

Benjamin A. Zamora Species in the Northern Intermountain Region.......................................................295

Benjamin Zamora Total Available Carbohydrates in Serviceberry After Late Summer

Thomas Gnojek and Fall Burning .....................................................................................................302

vii
Ronald E. Sosebee Long-Shoot/Short-Shoot Phenomenon in Woody Plants .......................................306

Ricardo Mata-González Aerial Biomass and Elemental Changes in Atriplex canescens and

Rubén Meléndez-González A. acanthocarpa as Affected by Salinity and Soil Water Availability ......................308

J. Jesús Martínez-Hernández

Community Ecology .........................................................................................................................................313

Suzanne Mayne Field Test of a New Australian Method of Rangeland Monitoring ..........................315

Neil West

K. T. Harper Quantifying Plant Diversity in Zion National Park, Utah .........................................318

Stewart C. Sanderson

E. Durant McArthur

Wendy Rosler Plant Diversity at Box-Death Hollow Wilderness Area,

Janet G. Cooper Garfield County, Utah .............................................................................................325

Renee Van Buren

Kimball T. Harper

Carl L. Wambolt Mountain Big Sagebrush Age Distribution and Relationships on the

Trista L. Hoffman Northern Yellowstone Winter Range ......................................................................330

Sherel Goodrich Mountain Big Sagebrush Communities on the Bishop Conglomerate

Allen Huber in the Eastern Uinta Mountains ..............................................................................336

Sherel Goodrich A Yellowbrush/Grass Community Type From the Uinta Mountains and

Robert M. Thompson Utah Plateaus .........................................................................................................344

Allen Huber

Darrell N. Ueckert Rate of Increase of Redberry Juniper (Juniperus pinchotii) Canopy

Robert A. Phillips Cover in Western Texas: Ecological and Economic Implications ...........................347

Joseph L. Petersen

X. Ben Wu

Stephan A. Nelle Ecological Implications of Using Goats for Control of Juniper in Texas .................352

Martha Martín-Rivera Habitat Improvement for Wildlife in North-Central Sonora, Mexico ........................356

Fernando Ibarra-Flores

Fred S. Guthery

William P. Kublesky, Jr.

Gustavo Camou-Luders

Jesus Fimbres-Preciado

Donald Johnson-Gordon

Field Trip .............................................................................................................................................................361

Howard C. Stutz Colorado Plateau Chenopod Field Trip ..................................................................363

viii
USDA Forest Service Proceedings RMRS-P-21. 2001 1

Anniversary Celebration

Genetics and Biodiversity

Disturbance Ecology

and Biodiversity

Ecophysiology

Community Ecology

Field Trip

USDA Forest Service Proceedings RMRS-P-21. 2001 2

Anniversary

Celebration

1

USDA Forest Service Proceedings RMRS-P-21. 2001 3

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

E. Durant McArthur is Project Leader and Research Geneticist, U.S.

Department of Agriculture, Forest Service, Rocky Mountain Research Station,

Shrub Sciences Laboratory, 735 North 500 East, Provo, UT 84606.

The Shrub Sciences Laboratory at 25 Years:

Retrospective and Prospective

E. Durant McArthur

Abstract—The Shrub Sciences Laboratory celebrated its 25th anniversary with the symposium documented by these proceedings and

a ceremony honoring people instrumental in its establishment: Mr.

A. Perry Plummer represented Forest Service Research and Development and Dr. Howard C. Stutz represented Brigham Young

University. The laboratory came into being because of the research

foundation in Western shrub ecosystems generated by USDA Forest

Service researchers and their colleagues and the need to carry on

programmatic research in vast Western shrublands. Since establishment of the laboratory, dozens of scientists and professionals

with technical and clerical support have conducted shrubland

ecosystem research and development centered on shrubland ecosystem ecology and experimental range management, including winter

livestock management on salt shrublands; seed quality testing and

production and seed and seedbed ecology and adaptation; genetic

variation, population biology, and systematics and taxonomy; breeding systems, hybridization, and hybrid zones; rangeland rehabilitation and restoration; equipment development, and cultural care of

wildland species; soil/plant interactions, pathology, entomology,

and mycorrhizae; nutritive quality, palatability, and wildlife habitat; and invasive weeds and weed biology. A continuing robust

research program is anticipated that will build on previous research

accomplishments, and will especially emphasize genetic variation

and plant material development, fire susceptible ecosystems, invasive weed control and biology, and the ecology and restoration of

ecosystems on the urban/wildland interface. Laboratory personnel

and collaborators have published nearly 800 titles during the past

quarter century; these are listed in the References section and in

appendix A.

Origin of Laboratory _____________

The Shrub Sciences Laboratory was officially opened

with appropriate fanfare on November 4–6, 1975, with a

shrub workshop for scientists and land managers; science

sessions featuring contributed and invited presentations

on shrub research (Stutz 1976); and a banquet, dedication, ribbon cutting, and open house. Some 350 people

attended these activities, which were held at the laboratory and at the Wilkinson Student Center of Brigham

Young University. Associate Deputy Chief of the Forest

Service Warren T. Doolittle, Intermountain Forest and

Range Experiment Station Director Roger R. Bay, and

Brigham Young University President Dallin H. Oaks presided at these functions that were cosponsored by the

Station, Brigham Young University, Utah Division of Wildlife Resources, Utah State University, and the Utah Section of the Society for Range Management. The program

steering committee included Howard C. Stutz, Professor,

Department of Botany and Range Science, Brigham Young

University; James P. Blaisdell, Assistant Director, Intermountain Forest and Range Experiment Station; Cyrus M.

McKell, Professor, Department of Range Science, Utah

State University; and Norman C. Hancock, Chief, Game

Management, Utah Division of Wildlife Resources.

The need for a laboratory dedicated to shrubland ecosystem research had been evident for some time (Blaisdell

1972). The Intermountain Forest and Range Experiment

Station (now part of the Rocky Mountain Research Station)

had been conducting research on the shrublands of the

Colorado Plateau, Great Basin, and associated mountains

beginning as early as 1912. The Intermountain Station had

established three experimental ranges in central and southern Utah, Great Basin, Desert, and Benmore (Astroth and

Frischknecht 1984; Clary and Holmgren 1982; Keck 1972;

Kitchen and McArthur 1996; McArthur and Monsen 1996),

and had active research units dealing with shrubland ecosystem research topics housed in office space with inadequate laboratory and greenhouse facilities in Ephraim and

Provo. Utah and Provo are centrally located in respect to the

vast shrublands of Western North America setting near the

juncture of the Rocky Mountain, Colorado Plateau, and

Basin and Range physiographic provinces. Within the U.S.

Department of Agriculture, Forest Service Research and

Development network of laboratories, the Shrub Sciences

Laboratory is unique in that it is the only location out of more

that 60 total research locations that is dedicated to research

on shrubland ecosystems. This is appropriate because up to

40 percent (1.8 x 106 km2

) of the conterminous 17 Western

United States is shrubland (Küchler 1964; McArthur and

Ott 1996).

The origin of the laboratory was documented, in part, in a

letter written to me on March 17, 1985, by retired (January 1,

1966) Forest Service Deputy Chief for Research V. L. Harper,

triggered by my presentation, “Building on Nature’s Diversity: Western Shrubs,” in the Forest Service Washington

Office Seminar Series, 1984–1985, on February 26, 1985:

I was much interested in the item about this seminar by

you in the 3-08 issue of The Friday Newsletter, published by

the F.S.

Among other things, it recalled to mind some history of the

Lab’s origin. I was doing a “Research Inspection” of the

Intermountain Station (about 1960) and one of the research

centers which Director Joe Pechanec and I visited was the

work on shrub research. After listening to the Project Leader’s

[A. Perry Plummer] presentation viewing some of the field

experiments, I turned to Joe Pechanec and said in effect...:
4 USDA Forest Service Proceedings RMRS-P-21. 2001

McArthur The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective

“Joe, maybe we ought to amend the Ten-year Research Program to include a new laboratory at Provo—a lab featuring

shrub research including genetics, etc.” Joe grinned broadly

and said “I hoped you would see this need.” He then produced

a memo outlining the justification for such a laboratory,

hopefully to be located on the grounds of Brigham Young

University. He further remarked, “I have prepared a speech,

which I can now cut short, giving a big pitch for the lab.” I told

Joe that I was personally acquainted with the president of the

university [Ernest L. Wilkinson] ... and had dealings with

him. “Why don’t we go to see him during this trip,” I said. Our

visit with the president was friendly and very encouraging.

He offered a long-term lease—free for the site for the building

and other cooperative aspects. Amending this projected research plan was not difficult. I simply added the Provo

location to the list of needed lab construction. The research

plan used only an overall figure for construction and I felt we

would not reach that figure anyway. From then on, while I

was Chief of Research, it was on the list that I gave Senator

Stennis, who in turn related it to the Senate in a speech and

to the Appropriation Sub-committee, at the proper time.

I am glad the Shrub Sciences Laboratory, unlike some

others that I got funds for from the Budget Bureau and/or

Congress, has not been abandoned by the current

Administration’s Budget cuts.

With the impetus generated by Deputy Chief Harper and

Station Director Pechanec through Forest Service administrative circles and the Congress and backed up by strong

Brigham Young University support, the laboratory became

a reality but not without some vicissitudes, for example,

annual appropriations for construction was impounded or

sequestered by the Administration until 1974 when $760,000

was authorized for construction; actual construction was

begun in October 1974 (fig. 1). The Utah Congressional

delegation of the time gave bipartisan support for the laboratory. Congressman Gunn McKay (D) was especially active

on behalf of the establishment of the laboratory (fig. 2);

Senators Frank Moss (D) and Wallace Bennett (R) and

Congressmen Sherm Lloyd (R) and Wayne Owens (D) were

supportive as well. The University was proactive in establishing the laboratory by providing the land for the laboratory, associated greenhouses, and support facilities both at

the laboratory site on the south edge of campus (735 North

Figure 1—Laboratory under construction (left) in February 1975 and in July 1999 (right). Photo on left by

Howard C. Stutz, on right by E. Durant McArthur.

500 East) and an ancillary site at 1325 East on 820 North

through long-term leases at the minimal legal cost of $1.

Originally, the laboratory was to be called the Shrub

Improvement Laboratory. However, Dr. Neil C. Frischknecht,

a charter Range Scientist and Team Leader in the Mineland

Reclamation Research Work Unit, raised the issue of the

name of the laboratory in a June 1975 memo:

...inasmuch as shrub improvement is essentially plant

breeding, it seems that one of the following titles would more

nearly reflect the scope of the research that will be done at the

new lab:...Shrub Research Laboratory, Shrub Science(s) Laboratory, Shrub-Range Improvement Laboratory. ...I have

learned that the FS plaque and letters “Shrub Improvement

Laboratory” are already on hand. If a change is in order, it is

far better to make it before the building is dedicated...

Dr. Frischknecht’s comment was recognized as meritorious,

and the more holistic name, Shrub Sciences Laboratory, was

selected and mounted on the front on the laboratory. Although my discipline is genetics, I believe it was a wise

decision. The steel cast letters from “improvement” not used

in “sciences” were presented to Dr. Blaisdell and Mr. Plummer

by Director Roger Bay, with accompanying jocular comments, in a meeting that I remember attending.

Importance of Shrubs and

Shrublands ____________________

The importance of shrub species and shrubland ecosystems in the Western United States and in other semiarid

areas gained considerable impetus from the activities leading up to the establishment of the Shrub Sciences Laboratory. An international symposium (Wildland Shrubs—Their

Biology and Utilization) was held in July 1971, at Utah State

University in Logan, drawing researchers and land managers from many countries (McKell and others 1972). I insert

a personal note: I was a postdoctoral research fellow at the

University of Leeds in England at the time. I recall seeing an

advertising flyer for the symposium and discussing with my

mentor, Mr. David Harberd, that the subject area of the

symposium was interesting and it would be nice to have an
USDA Forest Service Proceedings RMRS-P-21. 2001 5

The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective McArthur

opportunity to pursue a career in that area. Such are the

twists of fate that I had that opportunity shortly thereafter.

The symposium was followed several years later with a

textbook, The Biology and Utilization of Shrubs (McKell

1989). The extent, adaptation, and use of shrubs and ecosystems that they dominate together with the prospects of a

laboratory dedicated to shrub research that subsequently

became a reality also stimulated, in part, a series of workshops, symposia, and publications in Utah and surrounding

states and formation of the Shrub Research Consortium.

The Wyoming Shrub Ecology Workshop under the leadership of Drs. Herbert G. Fisser and Kendall L. Johnson of the

University of Wyoming ran for at least 17 years (1972 to

1988; Fisser 1990 lists all workshops). A similar Utah Shrub

Ecology Workshop, under the leadership of Drs. Kendall L.

Johnson and G. Allen Rasmussen of Utah State University

ran from 1981 to 1991 (Johnson 1990 lists workshops up to

that time; two subsequent workshops were held but the

proceedings were not published). The Shrub Research Consortium formed in 1983 with five institutional charter members

has expanded to a membership of 25 institutions (McArthur

and others 1999b; Tiedemann 1984) and has sponsored 11

wildland shrub symposia (more are in the planning stages)

with a diversity of wildland shrub biology themes.

Other period relevant publications include Wyoming

Shrubland Ecology, A Chronologic Supplemented Multiple

Source Annotated Bibliography (Fisser 1987), Shrubs of the

Great Basin, A Natural History (Mozingo 1987), The Sagebrush Ocean, A Natural History of the Great Basin (Trimble

1989), The Desert’s Past, A Natural Prehistory of the Great

Basin (Grayson 1993), and Natural History of the Colorado

Plateau and Great Basin (Harper and others 1994).

Twenty-Five Year Laboratory

Celebration ____________________

Two men were honored at a bust unveiling at the

beginning of the symposium and 25th year anniversary

documented in this publication. Mr. A. Perry Plummer

(fig. 3), long-time project leader of the Shrub Improvement and Revegetation Research Work Unit (now Shrubland Biology and Restoration RWU) of the Intermountain

Forest and Range Experiment Station (now Rocky Mountain Research Station) located at the Great Basin Experimental Range (= Great Basin Research Center), Ephraim,

Utah (McArthur 1991; Plummer 1972; 1977; Plummer

and others 1968) for many years prior to the establishment of the Shrub Sciences Laboratory, represented the

USDA Forest Service. Work by him and his group, including Utah Division of Wildlife Resources collaborators, on

big game range rehabilitation, especially using native

wildland shrubs, gave impetus and visibility to shrub

research. Dr. Howard C. Stutz (fig. 4), Emeritus Professor

of Botany and Range Science, Brigham Young University,

represented the University. Dr. Stutz was untiring in his

efforts as a liaison between the Utah Congressional delegation, the Forest Service, and the University during the

period from the addition of the laboratory to the Ten Year

Research Program in the early 1960s until the laboratory

became a reality. Dr. Stutz has a distinguished career in

Figure 2—Representative K. Gunn McKay (left),

Intermountain Station Director Roger R. Bay (center), and Brigham Young University President Dallin

H. Oaks (right), on the site of the future Shrub

Sciences Laboratory in 1974. Photo by Neil C.

Frischkecht.

plant genetics including many contributions to shrub

genetics, for example, Cutler 1996; Stutz 1978; Stutz and

others 1975, 1979, 1987; Stutz and Sanderson 1979, 1984,

1998; Stutz and Thomas 1964.

Dr. Daniel J. Fairbanks, Professor of Botany and Range

Science, Brigham Young University, sculpted the busts

and unveiled them with assistance from Mrs. Blanche

Plummer and her family, Dr. Howard Stutz and Mrs.

Mildred Stutz and their family, Rocky Mountain Research

Station Director Denver P. Burns, and Brigham Young

University President Merrill J. Bateman at the 25-year

anniversary ceremony at the beginning of the symposium.

The busts are now displayed in the front entrance of the

Shrub Sciences Laboratory. Director Burns and President

Bateman honored the 25-year celebration of the laboratory

and the contributions of Mr. Plummer and Dr. Stutz with

appropriate remarks. An open house at the laboratory was

held for those who attended the symposium as well as the

general public.
6 USDA Forest Service Proceedings RMRS-P-21. 2001

McArthur The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective

Staffing ________________________

At establishment time of the laboratory, the scientific

staff included elements of three Forest Service Research

Work Units (RWU): Shrub Improvement and Revegetation, Ecology and Management of Salt Desert Shrub Ranges,

and Mined-Land Reclamation. The first two units were

administered from the Shrub Sciences Laboratory, and the

third was headquartered in the Forestry Sciences Laboratory in Logan, Utah, but had detached members (Neil C.

Frischknecht and Robert B. Ferguson) stationed at the

Shrub Sciences Laboratory until Dr. Frishcknecht retired

in 1980 and Mr. Ferguson in 1983. The Ecology and Management of Salt Desert Shrub Ranges RWU continued at

the Shrub Sciences Laboratory until 1984, at which time

the unit was discontinued. Members of the unit were

reassigned to a new RWU—Riparian Stream Ecology and

Management—and moved to the Forestry Sciences Laboratory in Boise, Idaho, except for Fred J. Wagstaff who

remained at the Shrub Sciences Laboratory to manage the

Desert Experimental Range (DER). Dr. Wagstaff and the

Figure 3—Mr. A. Perry Plummer, Intermountain

Research Station Project Leader, instrumental in

establishment of Shrub Sciences Laboratory. Photo

courtesy of Mrs. Blanche Plummer.

Figure 4—Dr. Howard C. Stutz, Brigham Young

University Professor, tireless worker in behalf of

establishment of Shrub Sciences Laboratory. Photo

courtesy of Mrs. Mildred Stutz.

DER were transferred to administration of the Shrub

Improvement RWU in 1986. The Shrub Improvement and

Revegetation RWU changed its research emphasis to a

more holistic and ecosystem approach in 1993 and captured that move with a new name—Shrubland Biology and

Restoration. This unit’s core work has been at the Shrub

Sciences Laboratory since establishment of the lab in 1975,

but some individual scientists have been in detached locations from time to time. Most notably this included Stephen

B. Monsen and Nancy L. Shaw at the Boise Forestry

Sciences Laboratory. Mr. Monsen transferred to the Shrub

Sciences Laboratory in 1983; Dr. Shaw transferred to the

Riparian Stream Ecology and Management RWU in 1986.

The Shrubland Biology RWU has managed the Great Basin

Experimental Range (GBER) in Ephraim Canyon of the

Manti-La Sal National Forest as long as the unit and its

predecessors have been in existence. At the opening of the

laboratory, A. Perry Plummer and I were transferred from

the Great Basin Experimental Range to the new lab, but

the RWU has kept continued personnel presence at the

GBER. Cooperating scientists and other personnel from

the Utah Division of Wildlife Resources (UDWR) Wildlife
USDA Forest Service Proceedings RMRS-P-21. 2001 7

The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective McArthur

Habitat Restoration RWU had been closely integrated in

their work assignments with the Forest Service RWU. Both

units had been under the supervision of Mr. Plummer. The

administration eventually separated, but coordinated research activities have continued. The UDWR Wildlife Habitat Restoration unit maintained their administrative operation in Ephraim but have also had personnel stationed

at the Shrub Sciences Laboratory. Other agencies have had

a presence at the lab since the beginning. Table 1 lists

personnel who have been stationed at the Shrub Sciences

Laboratory and its attached Desert and Great Basin Experimental Ranges during the 1975 to 2000 timeframe. The

Benmore Experimental Range was deactivated as an experimental range in the early 1970s, and in any case, had no

one stationed permanently on the experimental range site.

Research Accomplishments ______

Research at the laboratory has covered and continues to

cover a broad range of topics related to wildland shrub

ecosystems, which is readily apparent in the list of publications (appendix A). However, I believe that the research

activities can be divided into nine principal areas of research

that are briefly highlighted in this section. The literature

citations for each research area are examples only and are

not complete—the complete list of activities is best understood and documented by the publications listed in appendix A and summarized in table 2. These publications are

principally inhouse, in other words, authored or coauthored

by Shrub Sciences Laboratory personnel, but also include

extramurally supported work including the integrated work

of Utah Division of Wildlife Resource collaborators and a

number of theses and dissertations funded and otherwise

abetted by the laboratory.

Shrubland Ecosystem Ecology and

Experimental Range Management

Research at the laboratory was given initial impetus by

research activities on the experimental ranges and other

experimental research and planting sites that preceded the

establishment of the laboratory. The Great Basin Experimental Range, perhaps better known as the Great Basin

Station with its ancillary outplantings and study plots, was

established in 1912, and has featured research on plant

adaptation, plant succession, nutrient cycling, revegetation, restoration ecology, watershed function, and game

habitat improvement over its long history, including the

time it has been administered out of the Shrub Sciences

Laboratory (Clary and Tiedemann 1986; Keck 1972;

Klemmedson and Tiedemann 1994, 1998b; McArthur and

Monsen 1996; McArthur and others 1999a; Plummer and

others 1968; Tiedemann and others 1987a; Tippets and

Anderson 1991; Walker and others 1996). The GBER is

located on the Manti-La Sal National Forest in and around

the Ephraim (Cottonwood) Canyon Drainage in Sanpete

County, Utah, and includes a diversity of vegetation communities over an elevational range from 6,800 to 10,000

feet.

The Desert Experimental Range was established in Pine

Valley, Millard County, Utah, in 1933, with most of the

area in the salt desert shrub community type, although

some areas extend to higher elevations into sagebrush and

pinyon-juniper communities. Research at the DER has

emphasized disturbance and successional processes in North

American cold desert plant communities, winter sheep

management in the cold desert, rodent ecology, pronghorn

biology and management, cryptobiotic soil crust ecology,

desertification, and avian and mammalian population dynamics (Alzerreca-Angelo and others 1998; Anderson and

others 1982a,b; Blaisdell and Holmgren 1984; Clary and

Beale 1983; Clary and Holmgren 1982; Harper and others

1996; Holmgren 1975; Kitchen and McArthur 1996; O’Neal

and others 1987; Tew and others 1997; Whisenant and

Wagstaff 1991).

The other experimental range administratively attached

to the Shrub Sciences laboratory was the Benmore Experimental Range (BER) that was deactivated as an experimental range about the time the laboratory was opened

and is administered by the Spanish Fork Ranger District of

the Uinta National Forest. The BER was established in the

middle 1930s in a sagebrush grass community in the

southeast corner of Rush Valley, Tooele County, Utah, and

emphasized crested wheatgrass (Agropyron cristatum)

seedings and livestock husbandry and production (Astroth

and Frischknecht 1984).

Aside from work performed on the experimental ranges,

other community and ecosystem scale research has emphasized autecology and synecology of important species and

baseline community ecology, emphasizing land areas and

plant and animal species for which land managers needed

information (Booth and others 1990; Davis 1990; Cibils and

others 1998; Ferguson and Medin 1983; Frischknecht 1975;

Goodrich 1984; Grover and DeFalco 1995; Harper and others

1990a, 1992; Hegerhorst and others 1988a; Holmgren 1984;

Kitchen and others 1999a; Liedolf and others 2000; McArthur

1994; McArthur and others 1989a, 1995a; McArthur and

Sanderson 1992a, 1999c; Medin 1984, 1986; Medin and

others 2000; Meyer 1997b; Meyer and Kitchen 1994a; Monsen

and Shaw 2000; Monsen and Stevens 1999b; Pendleton and

others 1995; Webb 1999; Weber and others 1985; Welch

1999; Welch and others 1995; Wood and Brotherson 1986;

Woodward and others 1984).

Another major ecological research effort headquartered

at the Shrub Sciences Laboratory is the Utah Division of

Wildlife Resources Range Trend Project. This effort has

been managed at the Shrub Sciences Laboratory since

1992. The effort is both interagency (U.S. Department of

Agriculture, Forest Service, Intermountain Region, and

Utah National Forests; and the U.S. Department of the

Interior, Bureau of Land Management, Utah State Office

and Utah Field Offices) and intra-agency (Utah Department of Agriculture and Food) in scope. The Range Trend

Program monitors over 700 permanent critical habitat big

game study sites on a repeating 5-year rotation. A wide

range of data is collected (nested frequency and cover of

vegetation, rock, litter, cryptogamic crusts, and bare ground;

nested frequency, quadrat frequency and cover of grasses

and forbs; cover, density, form class and vigor of shrubs and

trees; effective soil depth, average soil temperature, and

chemical and textural analysis of soil) as well as closeup and general view photos. Annual reports including

map direction to sites, narrative, and data are prepared
8 USDA Forest Service Proceedings RMRS-P-21. 2001

McArthur The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective

Table 1—Shrub Sciences Laboratory personnel, 1975 to 20001.

Personnel

Forest Service scientists

Philip A. Barker2 Warren P. Clary3 Robert B. Ferguson4

Neil C. Frischknecht2,3 Ralph C. Holmgren2,3 E. Durant McArthur2,3

Dean E. Medin Susan E. Meyer Stephen B. Monsen

David L. Nelson2,16 Burton K. Pendleton Rosemary L. Pendleton

A. Perry Plummer2,3 Arthur R. Tiedemann3 Charles F. Tiernan2

Fred J. Wagstaff Bruce L. Welch2

Professionals

A. Clyde Blauer5 Sherel Goodrich Stanley G. Kitchen

Carlos L. Lopez Kelly L. Memmott T. Blaine Moore5

Darren Naillon Stewart C. Sanderson

Other agency professionals

James N. Davis3,6 Mark Farmer6,7 Bruce C. Giunta5,6

Ashley Green6 Kent R. Jorgensen5,6 Scott Jensen5,6

Richard D. Porter8 Clare L. Poulsen5,6 Richard Stevens3,5,6

Jason L. Vernon5,6 Scott C. Walker3,5,6

Clerical/facilities

Steven F. Briggs9 Eulala Bulow5 Nancy Clark

Earl Daley Roma Jones1 Pat Ford10

Darlene Graham Roberta Leslie10 Norma Nielson2

Carla Oskoei Carolyn Osmond5,6 Charlotte Schuler

Ralph Sokolowski10 Karen Vance5 Chris Wade5,6

Mical Walker10 Sally Wolsey

Technicians

Stephanie L. Carlson Suzette Clement Susan C. Garvin

Gary L. Jorgensen5 John Kinney11 Nancy Mulligan

Ronald L. Rodriguez Heather Schijf Patti Schuttler

Temporaries

Bethany Allred David C. Anderson11 Kent Applegate6

Ganene Auger David G. Babbel Ben Baldwin6

Linda Bascom1 Maren C. Bauer Juie Beckstead

Greg Begera Barbara Behan Wendy Bird

Rick Black6 Mike Carter Joy D. Cedarleaf

Jeanne C. Chambers11 Dorcas Cheschelly Vearl Christensen

Richard Clark6 Linda K. Cluff Taylor Cox

Susan B. G. Debaene-Gill Jeff Duda11 John Fairchild6

Mark C. Grover Derek B. Hall Lorraine Hart11

Gary Holmberg6 Jesse Hunter Marie Jackson

Tracy L. C. Jacobson Bethanee Johnson David Kelley6

Celeste Kennard Sharlynn King Kim Lamb

Julia Liao Randell L. Leonard Bill Masslich

Thomas A. Monaco Joann Mudge Kathy Musso

Steve Otero Jeffery E. Ott Max Pierce

C. Lorenzo Pope Heidi Pullman Alisa P. Ramakrishnan

Doug Ramsey Alice Rhea Neil Roberts

Heidi Robbins Glade Sessions Matt Simmons

Jeffery Skousen6 Benton Smith Karl Sorensen

Lans Stavast Daniel Summers6 David Tarkalson

Tyler Thompson6 Bob Tuttle6 Craig Walker

Steven D. Warren6 Susan M. White Amber Whitworth6

Jerome Willy11 Dan Woodruff Roy D. Woodward

Annie Lane J. Yazzie Carrie York

Visiting scientists and professionals

Phil Allen12 Humberto Alzerreca-Angelo11 Donald Beale6,11

Abdul H. Belal Toupta Boguena Dianne Delany

Max Dunford John M. Emlen11 D. Carl Freeman13

Chu Ge-lin John H. Graham Ron Hacker

Roy O. Harniss5 Kimball T. Harper5,11 Mohamed Hassan

Dionne Maywald Kathy Miglia Gamel S. Mikel

Walter F. Muegggler12 Hamid Narjisse Mohamed A. Nasr

Brian E. Norton11 Jordan C. Pederson6 Gisbert Rinschede

(cont.)
USDA Forest Service Proceedings RMRS-P-21. 2001 9

The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective McArthur

Table 1—Cont.

Personnel

Stephen S. Rosenstock6 Burns R. Sabey Dave Stricklan14

Avi Schmida Courtney Smith11 Han Wang

SCSEPs

Geneva Ball Horacio Bausset Vergie Beaudoin

Doris Curtis Abbie Francom Julia Golding

Esther Humphries Lloyd Migliaccio Lorraine Mortensen

Brian Ruck Charles Shaw Dick Tennent5

Shari Veteto

Volunteers15

Imna Alabos11 Monica M. Bennion Ann Bickel

Cathleen Chamberlin-Graham Jerry Dunifer Scott Emlen11

Ursula Emlen11 Juan Escos11 Joel L. Kitchen

Ryan S. Kitchen Mont E. Lewis5 Curtis D. McArthur

Ted O. McArthur David Miglia Alex Parent

Lynden Porter Bettina Schultz Alan Smith

David Smith5 Chatelanine Stavast William A. Turner

Jeffery J. Vitale Diane Wagstaff Darren L. Welch

Michael B. Welch

Institutional Volunteers

Boy Scouts of America Earthwatch Utah Native Plant Society

1

The list of personnel is complete for permanent employees; some of the permanent employees started in temporary employee

positions. For Temporary and Senior Community Service Employment Program (SCSEP) employees the list is not complete but lists those

who worked for a year or more. 2Employees working at the Shrub Sciences Laboratory at the time it opened.

3

Project Leaders.

4

Bob Ferguson was transferred to the Shrub Sciences Laboratory within a month after it opened.

5Great Basin Experimental Range employees. Clyde Blauer and Blaine Moore were summer employees with permanent appointments

at Snow College. 6

Utah Division of Wildlife Resources employees.

7Utah Department of Agriculture and Food employee.

8

U.S. Departement of the Interior, Fish and Wildlife Service employee.

9

Steve Briggs was a technician before he became the facilities manager.

10Business Managers. 11Desert Experimental Range employees. 12Phil Allen was a UDWR technician before he became a visiting scientist from Brigham Young University. 13Carl Freeman was FS temporary before he became a visiting scientist from Wayne State University. 14Dave Stricklan was a Wildlife Biologist with the Uinta National Forest with special assigment for cooperation with Shrub Sciences

Laboratory Personnel. 15Only those volunteers who contributed at least 250 hours of time are listed, many other volunteers have made substantive

contributions. 16Since his retirement in 1996, David Nelson has contributed thousands of hours of work.

(Davis and others 1995a,b, 1996a,b,c,d, 1998a,b,c,d,e,f,

1999a,b, 2000a,b). The Range Trend Program data is also

housed on a web page: http://www.ag.state.ut.us/divisns/

mkt&cons/range.htm.

Seed Quality, Testing, and Production;

Seed and Seedbed Ecology and

Adaptation

A principal goal of work at the Shrub Sciences Laboratory has been to provide information about seeds of plants

that are used to restore or rehabilitate degraded rangeland

communities. To that end the laboratory has played and

continues to play an important role in setting standards for

the seeds in commerce used for wildland plantings (Allen

and Meyer 1986; Currans and others 1997; Meyer 1999;

Meyer and Kitchen 1995; Stevens and Meyer 1990; Young

and others 1995; and many publications in the Seed Technologists Newsletter and Newsletter of the Association of

Official Seed Analysts senior authored by Allen, Kitchen,

or Meyer). Other substantive work has emphasized seed

germination, collection, storage, processing, production,

and adaptation as well as seed and seedbed ecology for a

wide range of shrubland ecosystem species, for example,

sagebrush (Artemisia), saltbush (Atriplex), bitterbrush

(Purshia), rabbitbrush (Chrysothamnus), penstemon or

beardstongue (Penstemon), cheatgrass (Bromus) (Allen and

Meyer 1990, 1998; Allen and others 1987, 1995; Beckstead

and others 1996; Garvin and others 1996; Jacobsen and

Welch 1987; Jorgensen and Davis 1984; Kitchen and Meyer

1991; Kitchen and Monsen 1994; McArthur and others

1978c, 1987a; McArthur and Young 1999; Meyer 1989,

1992; Meyer and Allen 1999a,b; Meyer and Kitchen 1992,

1994b; Meyer and Monsen 1991, 1992; Meyer and others

1987g, 1989b, 1990, 1995b, 1997, 1998; Meyer and Paulsen

2000; Meyer and Pendleton 2000; Mikhiel and others 1992;

Monsen and Meyer 1990; Monsen and others 1985b; Noller

and McArthur 1986; Noller and others 1984; Plummer and

Jorgensen 1978; Plummer and Monsen 1977; Stevens and
10 USDA Forest Service Proceedings RMRS-P-21. 2001

McArthur The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective

Table 2—Summary of Shrub Sciences Laboratory publications, 1975 to 2000 (see appendix A for complete list).

Book Government Theses or ExtraYear Total Journal chapter Book serial Proceedings dissertations mural1

1975 14 6310312

1976 92001245

1977 14 4203142

1978 23 6 1 0 2 12 2 6

1979 20 6103829

1980 14 5104135

1981 33 16 003958

1982 20 14 103023

1983 53 11 1 3 9 24 5 7

1984 42 15 0 1 6 18 2 4

1985 41 17 0 1 6 15 2 8

1986 60 22 1 3 6 22 6 10

1987 47 21 2 2 2 17 3 4

1988 23 17 110133

1989 35 18 424702

1990 45 13 1 2 2 25 2 4

1991 12 11 001002

1992 28 14 214523

1993 21 7303714

1994 36 11 6 1 4 11 3 8

1995 34 11 1 1 4 12 5 7

1996 44 8 2 1 8 17 8 15

1997 16 8102233

1998 38 27 0 0 8 0 3 11

1999 48 11 1 2 4 30 0 14

2000 23 10 105524

Total 793 311 36 22 97 254 73 152

o 1

Extramural = no Shrub Sciences Laboratory Forest Service personnel authorship. Some lab personnel, for example, Steve Monsen and Stewart

Sanderson, had publications that are tied into the program prior to their assignment to the Shrub Sciences Laboratory and hence some of these

publications are scored as extramural or are listed in the regular reference section rather than in appendix A.

Jorgensen 1994; Stevens and others 1986, 1996; Wagstaff

and Welch 1991; Welch 1995, 1996, 1997b; Welch and

others 1996).

Shrub Sciences Laboratory personnel have made substantive contributions to the new Woody Plant Seed Manual as

principal authors of more than 20 included genera (Bonner

and Nisley, in review). This work has not yet been published,

but the material is being made available on a Web site as it

is prepared: <http:www.wpsm.net/>.

Plant Materials Development and Plant

Adaptation

Development of plant materials and their site adaptation was a principal reason for the establishment of the

laboratory and has remained an important part of the

research effort. Laboratory scientists were instrumental in

establishing various classes of wildland plant materials,

source identified, tested, selected, and cultivar for use in

rehabilitation plantings (McArthur 1988; Young 1995;

Young and others 1995; Welch 1994). We have formally

released for commercial development and use, with cooperators—mainly the Utah Division of Wildlife Resources,

Utah Crop Improvement Association, Upper Colorado Environmental Plant Center, and USDA Natural Resources

Conservation Service—15 separate germplasm lines:

‘Appar’ blue flax ( Linum perenne) (1980)

‘Rincon’ fourwing saltbush (Atriplex canescens) (1982)

‘Ephraim’ crested wheatgrass (Agropyron cristatum) (1983)

‘Paiute’ orchardgrass (Dactylis glomarata) (1983)

‘Immigrant’ forage kochia (Kochia prostrata) (1984)

‘Lassen’ antelope bitterbrush (Purshia tridentata) (1984)

‘Hatch’ winterfat (Ceratoides lanata) (1985)

‘Cedar’ Palmer penstemon (Penstemon palmerii) (1985)

‘Summit’ Louisiana sagewort (Artemisia ludoviciana) (1986)

‘Hobble Creek’ mountain big sagebrush (Artemisia tridentata

ssp. vaseyana) (1987)

‘Gordon Creek’ Wyoming big sagebrush (A. tridendata ssp.

wyomingensis) (1992)

‘Pine Valley Ridge’ black sagebrush (A. nova) (1994)

‘Timp’ northern sweet vetch (Hedysarum boreale) (1994)

‘Maybell’ antelope bitterbrush (Prushia tridentata) (1994)

‘Umatilla’ snow buckwheat (Eriogonum niveum) (1997)

Several other plant materials, under current evaluation,

are candidates for release for various reclamation and restoration applications including bluebunch wheatgrass

(Pesudoroegneria spicata) (Anatone, WA); Thurber’s

needlegrass (Stipa thurberiana) (Boise, ID), Sandberg bluegrass (Poa secunda) (Mountain Home, ID), additional lines

of forage kochia (Kochia prostrata), Lewis flax (Linum

perenne) (Scipio, UT), plains silver sagebrush (Artemisia

canassp. cana) (Sheridan, WY), a small burnet (Sanguisorba
USDA Forest Service Proceedings RMRS-P-21. 2001 11

The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective McArthur

minor) synthetic, sagebrush hybrids (Artemisia species and

subspecies) (for fire tolerance), and several native forbs.

Some of the key references for the plant material development and release are Carlson and McArthur 1985; Carlson

and others 1991; Kitchen 1995; McArthur 1988; McArthur

and others 1984b; Monsen and Stevens 1985; Shaw and

Monsen 1986; Stevens and Monsen 1985b, 1988a,b; Stevens

and others 1985a; Welch and others 1986a, 1992a, 1994; and

unpublished data on file at the Shrub Sciences Laboratory.

In the process of evaluating plant materials and determining their potential for use in rehabilitation and restoration

outplanting, adaptation and evaluation tests have been conducted, for example, Belal and others 1993; Davis 1983;

Dewey and Plummer 1980; Ferguson 1983; Ferguson and

Frischknecht 1985; Frischknecht 1983; Frischknect and

Ferguson 1984; McArthur 1981, 1983; McArthur and others

1983b, 1995b, 1996; McArthur and Welch 1982; Monsen

1983, 1987; Monsen and Anderson 1993; Monsen and

Christensen 1976; Monsen and Plummer 1978; Plummer

1977; Shaw and Monsen 1983b; Tiedemann and Driver 1983;

Welch and McArthur 1986a. Laboratory personnel and university colleagues have been involved with a series of studies

on current and predictive adaptation as determined by physiological fitness by using measures of respiration, metabolism,

and temperature (Criddle and others 1994; Frank and others

1986; Jones and others 1999; McArthur and others 1998a;

Monaco and others 1996; Smith and others 1999).

Genetic Variation, Population Biology,

and Systematics and Taxonomy

To better manage, protect, and use wildland shrub species

(and associated nonshrub species), their taxonomic status

and relationships need to be understood. Many of these

species were poorly defined and their inter- and intrapopulation dynamics unknown in 1975. Much progress has been

made to better understand these issues by work performed by

laboratory personnel and collaborators, but much work remains to be done. Many new molecular-based techniques

have become available in recent years (Judd and others 1999).

Cytological research by Shrub Sciences Laboratory personnel on big sagebrush and its relatives (= subgenus

Tridentatae of Artemisia) (McArthur and others 1981;

McArthur and Plummer 1978; McArthur and Sanderson

1999a); other Artemisia (McArthur and Pope 1979), the

saltbushes (Atriplex) (Sanderson and Stutz 1994a; Stutz

and others 1979; Stutz and Sanderson 1979, 1984, 1998),

greasewood (Sarcobatus) (Sanderson and others 1999),

and spineless hopsage (Grayia brandegei) (Stutz and others 1987) has documented intriguing polyploidy, some of it

related to habitat conditions (McArthur and Sanderson

1999a; Sanderson and others 1989). Other substantive

cytological research (first or most substantive records known

for the groups) has been done for bitterbrush (Purshia),

cliffrose (Cowania), Apache plume (Fallugia), mountain

mahogany (Cercocarpus), and other rosaceous shrubs

(McArthur and others 1983c; McArthur and Sanderson

1985).

Chemotaxonomic work based on macromolecules including phenolics, terpenoids, isoenzymes, and DNA have been

used to clarify population biology, species and subspecies

relationships among many plant groups (Leonard and

others 1981; McArthur and others 1998c) including the big

sagebrush group (subgenus Tridentatae of Artemisia)

(Hanks and others 1973; McArthur and others 1981, 1988b,

1998b,c; Stanton and others 2001; Stevens and McArthur

1974; Welch and McArthur 1981), rabbitbrush (Chrysothamnus) (Hanks and others 1975; McArthur and others 1978a;

Hegerhorst and others 1987a), saltbush (Atriplex)

(McArthur and others 1986b; Sanderson and others 1987,

1988, 1990; Sanderson and Stutz 1984), Gambel oak (Quercus gambelii) (Pendleton and others 1985), and rust fungi

(Volger and others 1996).

Comparative studies of populations and individuals grown

in uniform gardens have yielded results that have clarified

variation and relationships and facilitated breeding and

hybridization studies for several plant groups including

sagebrush (Behan and Welch 1986; Criddle and others 1994;

McArthur and Welch 1982; Welch and McArthur 1979b,

1981, 1986a), rabbitbrush (Hegerhorst and others 1987a,c;

Bhat and others 1990a,b), bitterbrush and cliffrose (Criddle

and others 1994; Pendleton and McArthur 1994; Welch and

others 1983a), saltbush (McArthur and others 1983b;

Pendleton and others 1992a, 1994; Welch and Monsen 1981,

1984), and forage kochia (Davis and Welch 1984, 1985;

McArthur and others 1996; Pendleton and others 1992b;

Welch and Davis 1984).

Laboratory personnel have been active in clarifying and

popularizing taxonomic placement and values of shrubs and

associated species in general terms in floras (Goodrich 1984;

1986a; 1986b; Goodrich and Neese 1986; Welsh and others

1987), for specific groups of plants, for example, composite

(McArthur and others 1979a), chenopod (Blauer and others

1976; McArthur and Sanderson 1984; Sanderson and Stutz

1994b), and rose family (Blauer and others 1975) shrubs,

willows (Goodrich 1983), sagebrush (McArthur 1979, 1983,

1994; McArthur and Goodrich 1986; McArthur and others

1981; Welch and McArthur 1990), rabbitbrush (McArthur

and others 1978a; McArthur and Meyer 1987; Weber and

others 1985, 1993), fourwing saltbush (Freeman and

McArthur 1989), bearclaw poppies (Meyer 1997a),

Sphaeromeria (McArthur and others 1989a, 1998c), and

several other plant groups (Goodrich 1985, 1986; Goodrich

and others 1985a).

Laboratory personnel have also formally named and otherwise systematically treated several plant taxa (Atwood

and others 1984; Chu and others 1991; Goodrich and others

1985b; Goodrich and Welsh 1983; McArthur and others

1981; Stutz and others 1993, 1994, 1997, 1998; Stutz and

Sanderson 1998; Winward and McArthur 1995).

A series of studies were performed to determine the extent

and variation of resin and rubber products in rubber rabbitbrush (Chrysothamnus nauseosus). Populations and individuals were found to differ as were rubber and resin

concentrations, on a seasonal basis (Bhat and others 1989,

1990b; Hegerhorst and others 1987b,c; 1988a,b; Weber and

others 1985, 1989, 1993).

Breeding Systems, Hybridization,

and Hybrid Zones

An important factor in the study of population biology,

systematics, and natural hybridization and controlled

hybridization is a clear understanding of breeding and
12 USDA Forest Service Proceedings RMRS-P-21. 2001

McArthur The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective

pollination systems. Work at the laboratory has been fundamental in clarifying and describing breeding systems in

several ecologically important wildland shrub ecosystem

species complexes including sagebrush (Artemisia), rabbitbrush (Chrysothamnus), saltbush (Atriplex), bitterbrushcliffrose (Purshia-Cowania), blackbrush (Coleogyne), spiny

hopsage (Grayia spinosa), beardstongue (Penstemon), and

flax (Linum) (McArthur 1989a; Pendleton and others 1989).

The big sagebrush species complex (subgenus Tridendatae

of Artemisia) is perhaps the vegetation icon of the Western

United States inasmuch as members of this group are

widespread, dominant, and woven into history and culture

(Trimble 1989). Work performed by Shrub Sciences Laboratory personnel has demonstrated that taxa (populations,

subspecies, species) of these plants outcross but are also selffertile, that hybridization has been important in evolutionary development of the group, and that hybridization may

be important in management and recovery (from fire and

other degradation processes) of the group (McArthur and

others 1979a, 1988b, 1998b). In a series of studies examining growth and fitness in narrow hybrid zones and hybridization dynamics, laboratory personnel and colleagues have

shown the likelihood that hybridization processes are important in the diversification and success of this plant group

(Byrd and others 1999; Freeman and others 1991, 1995,

1999a,b; Goodrich and others 1985b; Graham and others

1995, 1999, 2001; McArthur and Goodrich 1986; McArthur

and others 1988b, 1998a; McArthur and Sanderson 1999b;

Messina and others 1996; Smith and others 1999; Wang and

others 1997, 1998, 1999; Weber and others 1994; Winward

and McArthur 1995). This series of studies has provided

strong support for a hybrid zone model, Bounded Hybrid

Superiority Hybrid Zone Model (Arnold 1997; Moore 1977),

that posits the superiority of hybrid plants over parental

plants but only in the hybrid zone, in contrast to competing

hybrid zone models. The model can account for the abundance

and apparent stability of numerous Tridentatae hybrid zones.

The breeding systems of chenopod family shrubs are another area in which laboratory personnel and collaborators

have made fundamental discoveries and contributions to the

scientific literature. Like the sagebrushes, these plants are

often landscape dominants or are prominent community

members and include species with wide distributions that are

often important species in land management issues. These

plants are monecious or dioecious and wind pollinated

(McArthur and Sanderson 1984). Laboratory personnel and

collaborators have shown that many saltbush species, especially fourwing saltbush (A. canescens) have an adaptive

breeding system that incorporates environmental factors, for

example, moisture and temperature into a flexible, yet genetically controlled, sexual system that enhances reproductive

fitness in a patchy environment (Freeman and McArthur

1982, 1984, 1989; Freeman and others 1984, 1993a,b;

McArthur 1977; McArthur and Freeman 1982; McArthur and

others 1992; Pendleton and others 1992a, 1994). Knowledge

of these sexual systems has practical implications in terms of

nutrition, palatability, and seed production issues for management (Cibils and others 1998; Maywald and others 1998;

McArthur and others 1978c; Tiedemann and others 1987b).

Spineless hopsage (Grayia brandegei) has been shown to have

an unusual breeding system, heterodichotamy, that like the

trioecious system of Atriplex canescens (McArthur and others

1992; Freeman and others 1993b) appears to be adaptive to a

patchy, resource-poor environment and may be on an evolutionary pathway to dioecy (Pendleton and others 1988, 2000b).

This system may be useful in better understanding general

breeding patterns in a wider context as well (Freeman and

others 1981, 1997).

Breeding systems of other plants have been studied to

better understand, manage, and use important shrubland

ecosystem species. These include rabbitbrush (Chrysothamus)

(McArthur and others 1978a; Meyer 1997b), bitterbrush and

cliffrose (Purshia/Cowania) (Davis 1983; McArthur and others 1983c; Meyer and Pendleton 2000; Pendleton and McArthur

1994), blackbrush (Coleogyne) (Pendleton and Pendleton 1998),

blue flax (Linum perenne and L. lewisii) (Kitchen 1995; Meyer

and Kitchen 1994a; Pendleton and others 1993—References

Section, not appendix A), and cheatgrass (Bromus tectorum)

(Beckstead and others 1996; Hemming and others 1999;

Meyer and Allen 1999a,b; Meyer and Ramakrishnan, unpublished data, Shrub Sciences Laboratory).

Rangeland Rehabilitation and Restoration,

Equipment Development, and Cultural

Care of Wildland Species

Techniques, demonstrations, and review for wildland

rehabilitation and restoration including equipment development and use, application of herbicides, and cultural

care of species used for wildland rehabilitation and restoration has been a major, continuing effort by Shrub Sciences Laboratory personnel and collaborators, especially

the Utah Division of Wildlife Resources Habitat Restoration Unit. The principal efforts have been on disturbed sites

such as minelands, domestic and big game rangelands,

roadside disturbances, and so forth, and are documented

and detailed in Blauer and others 1993; Clary and Johnson

1983; Clary and others 1985b,c,d; Davis and Harper 1990;

Ferguson and Frischkneck 1981, 1985; Frischknecht 1978b;

Frischknecht and Ferguson 1979; Giunta and others 1975;

Hall and others 1999; Luke and Monsen 1984; McArthur

and others 1978b, 1987b, 1990a, 1995b, 2000; McArthur

and Sanderson 1996; Monsen 1978, 1984, 1987, 2000;

Monsen and Kitchen 1994; Monsen and Meyer 1990; Monsen and Turnipseed 1990; Monsen and others 1985b, 1992,

1996; Monsen and Richardson 1984; Monsen and Shaw

1983a,b, 1986, 1996, 1999; Monsen and Stevens, in review

(see References Section, not appendix A); Plummer 1976,

1977; Roundy and others 1995; Sabey and others 1990;

Shaw and Monsen 1984, 2000; Skousen and others 1986;

Stevens 1978, 1994, 1999a,b; Stevens and McArthur 1990;

Stevens and Walker 1998; Tiedemann and Lopez 1983; Van

Epps 1978; Walker and others 1995; Welch, in review (see

References section, not appendix A); Whisenant and Clary

1986, 1987; and Whisenant and McArthur 1989.

Several studies have dealt with the economics of the

rehabilitation processes. These have been of a general nature (Clary 1983a; Wagstaff 1983b,c,d; 1986d; Wagstaff and

Pope 1987; Wagstaff and Reesman 1989) and more specific.

Specific economic analyses have been presented for individual projects (Pope and Wagstaff 1987a,b), oakbrush

(Wagstaff 1985), riparian (Wagstaff 1986c), pinyon and

juniper (Clary and Wagstaff 1987; Wagstaff 1987), and
USDA Forest Service Proceedings RMRS-P-21. 2001 13

The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective McArthur

sagebrush community management (Wagstaff 1986a), as

well as for prescribed fire application (Pope and Wagstaff

1990) and big game use on private lands (Nielsen and others

1985, 1986).

Soil/Plant Interactions, Pathology,

Entomology, and Mycorrhizae

Plant interactions with fungi, insects, soil, and other

factors have been a continuing area of study at the Shrub

Sciences Laboratory. These interactions are often positive

for plants but can be negative as well. A considerable

amount of work on soil crusts and mycorrhizae has demonstrated many positive interactions with microorganisms

and several shrubland ecosystem plant species; these interaction are often crucial to community health (Anderson and

others 1982a; Belnap 1993, 1996; Belnap and Gardner 1993;

Belnap and Harper 1995; Belnap and others 1996; Buttars

and others 1998; Harper and Pendleton 1993; Pendleton

2000; Pendleton and others 1999, 2000a; Pendleton and

Smith 1983; Pendleton and Warren 1996). Other studies

performed on plant soil interactions include some with a

community focus (Klemmedson and Tiedemann 1998a,b;

Kitchen and Jorgensen 1999) and on Gambel Oak (Quercus

gambelii) (Clary and Tiedemann 1986; Tiedemann and

others 1987a) and big sagebrush (Artemisia tridentata)

(Wang and others 1998, 1999; Welch 1997b; Welch and

Jacobson 1988).

Nitrogen fixation in the semiarid systems dominated by

wildland shrubs is an important ecological function provided by several species. The actinorhizal (Frankia) relationships with antelope bitterbrush (Purshia tridentata),

Stansbury cliffrose (Cowania stansburiana), curlleaf mountain mahogany (Cercocarpus ledifolius), and buckbrush

(Ceanothus) have been documented by Shrub Sciences Laboratory personnel and colleagues (Nelson 1983; Nelson and

Lopez 1989; Nelson and Schuttler 1984; Wood and others

1989).

A sustained effort has been made in studying wildland

shrub ecosystem disease and insect relationships. Research

performed on plant diseases includes work on big sagebrush (Artemisia tridentata) (Hess and others 1985; Nelson 1987; Nelson and Krebill 1981; Nelson and Sturgess

1986; Sturgess and Nelson 1986; Welch and Nelson 1995),

antelope bitterbrush (Purshia tridentata) (Nelson 1987),

saltbushes (Atriplex) (Ramsey and others 1995), Utah juniper (Juniperus osteospermus) (Bunderson and others 1986a),

pines (Pinus) (Nelson 1982; Nelson and Krebill 1982), and

quaking aspen (Populus tremuloides) (Harniss and Nelson

1984). A new series of studies is exploring the feasibility of

biological control of cheatgrass (Bromus tectorum) by exploiting the interactions of the headsmut, Ustilago bullata,

with cheatgrass (Meyer and others 2000b, 2001—see Reference Section not appendix A). General relationships on

wildland shrub insect interactions have been reviewed

(Tiernan 1978, 1980), and a general index on wildland

shrub insect relationships has been published (Haws and

others 1988). Specific documentation on the insects of

forage kochia (Kochia prostrata) (Moore and others 1982),

the insect-induced galls of big sagebrush (Artemisia tridentata) (Graham and others 2001—see Reference section not

appendix A), rubber rabbitbrush (Chrysothamnus nauseosus) (McArthur 1986; McArthur and others 1979b), and

curlleaf mountain mahogany (Cercocarpus ledifolius) (Tiedemann and Furniss 1985) defoliator have been provided.

Shrub die-offs, winter injury, and other environmental

problems in managing and understanding wildland shrub

ecosystems have been studied by laboratory personnel and

collaborators. The primary causes of these phenomena are

explored and documented (Haws and others 1990, 1993;

McArthur and others 1988a; Nelson and others 1989, 1990a,b;

Wallace and Nelson 1990; Walser and others 1990; Weber

and others 1995, 1999; Van Epps 1975).

Nutritive Quality, Palatability,

and Wildlife Habitat

One of the principal values of shrubs and shrubland

ecosystems is habitat, including feed value for wildlife and

domestic animals. Quantifying nutritive value and palatability of shrub species and other plants has been a substantive contribution of the research conducted at the Shrub

Sciences Laboratory. Some early work quantifying the differential palatability of big sagebrush (Artemisia tridentata

populations and subspecies) (Hanks and others 1971; Scholl

and others 1977) stimulated followup documentation and

hypothesis testing. Some general review and synthesis of

nutritive quality in wildland shrub ecosystems are Belal and

others 1993; Provenza and others 1987b; Tiedemann and

others 1984a; and Welch 1981, 1989, 1994. Research on the

preference and nutrititive quality of big sagebrush to a

number of consuming animals has been completed (Elderkin

and others 1986; Hobbs and others 1986; Welch 1983a, 1999;

Welch and McArthur 1979b, 1981, 1986b; Welch and others

1981, 1983b, 1987, 1991; Welch and Pederson 1981; White

and others 1982a). The concern that essential oils

(monoterpenoids) were a serious deterrent to digestion and

compromised the nutritive quality of big sagebrush has been

shown to be moot inasmuch as animals such as mule deer,

pygmy rabbits, sage grouse, and other herbivores are able to

ameliorate the high essential oil concentrations and thereby

take advantage of the species’ high nutrient content

(Cedarleaf and others 1983; Clary and others 1988; Cluff

and others 1982; Pederson and Welch 1982; Welch and

others 1982, 1983a,c; 1989; White and others 1982b). Likewise the nutritive values of black sagebrush (Artemisia

nova) have been documented (Behan and Welch 1985, 1986;

Welch and others 1981). Other species and groups of plants

that have been studied by laboratory personnel from a

nutrition perspective include the saltbushes (Atriplex

canescens and other Atriplex species) (Cibils and others

1998; Maywald and others 1998; Sanderson and others

1987; Welch 1978; Welch and Monsen 1981, 1984), rabbitbrush (Chrysothamnus species) (Hanks and others 1975;

Bhat and others 1990b; Goodrich and others 1999a), and

several other species (Davis and Welch 1985; Monsen and

others 1990; Pendleton and others 1992c; Welch and Andrus

1977; Welch and Davis 1984; Welch and others 1983b; Welch

and Wagstaff 1992).

A series of reports have dealt with quality of habitats for

animals, for example, the Utah Division of Wildlife Resource

Range Trend Studies (Davis and others, several references,
14 USDA Forest Service Proceedings RMRS-P-21. 2001

McArthur The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective

1995 to 2000), pronghorn antelope (Clary and Beale 1983),

salt desert game ranges (McArthur and others 1978b), mule

deer (Rosenstock and others 1989), domestic sheep and elk

(Beck and others 1996a,b), cattle (Vallentine and Monsen

1990), and desert tortoise (McArthur and others 1994).

Invasive Weeds and Weed Biology

Invasive weeds are a serious problem on Western wildlands. These pests may well be the most serious problem

facing land managers on Western public lands (Cronk and

Fuller 1995; D’Antonio and Vitousek 1992). Shrub Sciences

Laboratory personnel have contributed to the understanding of this problem and are seeking solutions and facilitating

scientific exchange (Buchanan and others 1978; Harper and

others 1996; Kitchen and Jorgensen 1999; McArthur and

others 1990b; Monsen and Kitchen 1994; Monsen 1994b;

Monsen and Shaw 1997). Research has been conducted on

cheatgrass (Bromus tectorum), bur buttercup (Ranuculus

testiculatus), halogeton (Halogeton glomeratus), rush skeleton weed (Lygodesmis juncea), squarrose knapweed (Centaurea virgata), and salt cedar (Tamarix ramosissima). The

work on cheatgrass has employed competition (Giunta and

others 1975; McArthur and others 1990a; Monsen and

Turnipseed 1990) as well as biocontrol (Meyer and others

2000b, 2001, see Reference section and appendix A), herbicidal control (Shaw and Monsen 2000), and wide array of

germination studies (Allen and others 1995; Bauer and

others 1998; Beckstead and others 1995, 1996; Meyer and

Allen 1999a,b; Meyer and others 1997) of cheatgrass. Other

more general work on a variety of weed problems has

emphasized control through competition (Davis and Harper

1990; Stevens and McArthur 1990) and herbicides (Stevens

and Walker 1998).

Technology Transfer Activities ____

The Shrub Sciences Laboratory has been a leader in

promoting scientific exchange by sponsoring and cosponsoring symposia, workshops, seminars, tours, discussions, and

lectures, and by hosting short- and long-term visits of extramural personnel (table 2) as well as sending its personnel to

participate in local, national, and international science meetings and to visit other research and management sites.

Several outcomes of these activities are documented by

publications of these proceedings:

Johnson 1983

Tiedemann and Johnson 1983

Monsen and Shaw 1983b

Wagstaff 1983e

Johnson 1984

Tiedemann and others 1984b

Carlson and McArthur 1985

Johnson 1985

McArthur and Welch 1986b

Johnson 1987

Provenza and others 1987b

Wallace and others 1989

Johnson 1990

McArthur and others 1990b

Clary and others 1992

Monsen and Kitchen 1994

Roundy and others 1995

Barrow and others 1996

McArthur and others 1999b

Monsen and Stevens 1999b

A perusal of the publications in appendix A demonstrates that Shrub Sciences personnel have participated

in many widespread venues. The laboratory serves as the

headquarters of two research consortia (Shrub Research

Consortium and Intermountain Consortium for Arid Land

Research) that foster coordinated research (Tiedemann

1984; McArthur 1991). Personnel have a continuing history of activity in professional societies, especially in the

Society for Range Management and the Utah Native

Plant Society, and in various other formal and informal

outreach activities.

The Future _____________________

Currently, the Shrub Sciences Laboratory houses the

Rocky Mountain Research Station Shrubland Biology and

Restoration Research Work Unit. The unit’s mission is to

“develop knowledge, plant materials, and technology for

successful long-term restoration of diverse shrubland plant

communities to meet resource needs and values.” Three

research problems are identified and approved to accomplish this mission:

1. Develop basic knowledge about the genetic makeup,

population dynamics, and biology of selected shrubland

species deemed important for ecologically sound restoration

efforts.

2. Develop and establish appropriate seed sources and

effective techniques for establishing high diversity shrubland communities from seed.

3. Develop a better understanding of community-level

consequences of past and present management practices

and provide recommendations consistent with ecosystem

management policies.

The unit accomplishes these goals, in part, with tight working relationships with Brigham Young University, where its

scientists have adjunct faculty status, and with other universities and agencies. Especially close working relationships are in place with units of the National Forest System,

the Bureau of Land Management, and the Utah Division of

Wildlife Resources. Two units of the UDWR are close cooperators: the Range Trend Analysis Unit is collocated at the

Shrub Sciences Laboratory, and UDWR Wildlife Habitat

Improvement Unit in Ephraim, Utah, is collocated with the

RMRS Great Basin Experimental Range.

As research work at the Shrub Sciences Laboratory moves

into its second quarter century, the team of researchers

anticipates that the research activities will build on the

foundation of established research by continuing emphasis

in plant materials research, restoring and rehabilitating

damaged ecosystems, and documenting, capitalizing, and

manipulating genetic variation. The team will be proactive

in seeking new research opportunities and partnerships

within the scope of its research mission and especially, in the
USDA Forest Service Proceedings RMRS-P-21. 2001 15

The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective McArthur

near term, will give added emphasis to work in fire susceptible ecosystems, on invasive weed control and biology, and

on the ecology and restoration of ecosystems on the urban

interface.

Acknowledgments ______________

I thank my colleagues, especially Nancy Shaw, Stewart

Sanderson, Stan Kitchen, and Richard Stevens, for review

and proofreading. I tried to list all appropriate publications

and personnel. If errors and omissions remain, they are mine.

References _____________________

See appendix A for Shrub Sciences Laboratory references,

1975–2000.

Arnold, M. L. 1997. Natural hybridization and evolution. New York:

Oxford University Press. 215 p.

Blaisdell, J. P. 1972. Needs and opportunities for shrub research in

the Western United States. In: McKell, C. M.; Blaisdell, J. P.;

Goodin, J. R., tech. eds. Wildland shrubs—their biology and

utilization: an international symposium; 1971 July 2–16; Logan,

UT. Gen. Tech. Rep. INT-1. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Forest and Range

Experiment Station: 409–413.

Bonner, F. T.; Nisley, R. G., comps. [In review]. Woody plant seed

manual. Washington, DC: U.S. Department of Agriculture, Forest Service.

Cronk, Q. C. B.; Fuller, J. L. 1995. Plant invaders, the threat to

natural ecosystems. London: Chapman and Hall. 241 p.

Cutler, S. N. 1996. BYU professor reclaims lost lands. Brigham

Young Magazine. 50(3): 10–11.

D’Antonio, D. M; Vitousek, P. M. 1992. Biological invasions by exotic

grasses, the grass-fire cycle, and global change. Annual Review of

Ecology and Systematics. 23: 63–88.

Fisser, H. G. 1987. Wyoming shrubland ecology. Science Monograph

49. Laramie: University of Wyoming, Wyoming Agricultural

Experiment Station. 661 p.

Fisser, H. G., ed. 1990. Wyoming shrublands: aspen, sagebrush, and

wildlife management: proceedings of the seventeenth Wyoming

shrub ecology workshop; 1988 June 21–22; Jackson, WY. Laramie:

University of Wyoming, Department of Range Management. 76 p.

Graham, J. H.; McArthur, E. D.; Freeman, D. C. 2001. Narrow

hybrid zone between two subspecies of big sagebrush (Artemisia

tridentata: Asteraceae). XII. Galls on sagebrush in a reciprocal

transplant garden. Oecologia. 126: 239–246.

Grayson, D. K. 1993. The desert’s past, a natural prehistory of the Great

Basin. Washington, DC: Smithsonian Institution Press. 356 p.

Hanks, D. L.; Brunner, J. R.; Christensen, D. R.; Plummer, A. P.

1971. Paper chromatography for determining palatability differences in various strains of big sagebrush. Res. Pap. INT-101.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Forest and Range Experiment Station. 9 p.

Hanks, D. L.; McArthur, E. D.; Stevens, R.; Plummer, A. P. 1973.

Chromatographic characteristics and phylogenetic relationships

of Artemisia, section Tridentatae. Res. Pap. INT-141. Ogden, UT:

U.S. Department of Agriculture, Forest Service, Intermountain

Forest and Range Experiment Station. 24 p.

Harper, K. T.; St. Clair, L. L.; Thorne, K. H.; Hess, W. M., eds. 1994.

Natural history of the Colorado Plateau and Great Basin. Niwot:

University of Colorado Press. 294 p.

Johnson, K. L., ed. 1983. Proceedings of the first Utah shrub ecology

workshop; 1981 September 9–10; Ephraim, UT. Logan: Utah

State University, College of Natural Resources. 50 p.

Johnson, K. L., ed. 1984. Proceedings of the second Utah shrub

ecology workshop; 1982 September 15–16; Fillmore, UT. Logan:

Utah State University, College of Natural Resources. 37 p.

Johnson, K. L., ed. 1985. Proceedings of the third Utah shrub

ecology workshop; 1983 August 30–31; Provo, UT. Logan: Utah

State University, College of Natural Resources. 61 p.

Johnson, K. L., ed. 1987. Proceedings of the fourth Utah shrub

ecology workshop, the genus Chrysothamnus; 1986 September

17–18; Logan, UT. Logan: Utah State University, College of

Natural Resources. 59 p.

Johnson, K. L., ed. 1990. Proceedings of the fifth Utah shrub

ecology workshop, the Genus Cerocarpus; 1988 July 13–14;

Logan, UT. Logan: Utah State University, College of Natural

Resources. 105 p.

Judd, W. S.; Campbell, C. S.; Kellogg, E. A.; Stevens, P. F. 1999.

Plant systematics, a phylogenetic approach. Sunderland, MA:

Sinauer Associates, Inc. 464 p.

Keck, W. M. 1972. Great Basin Station—sixty years of progress in

range and watershed research. Res. Pap. INT-118. Ogden, UT:

U.S. Department of Agriculture, Forest Service, Intermountain

Forest and Range Experiment Station. 48 p.

Küchler, A. W. 1964. Manual to accompany the map, potential

natural vegetation of the conterminous United States. Special

Pub. 36. New York: American Geographical Society. 116 p plus

1:3,168,000 scale map.

McKell, C. M., ed. 1989. The biology and utilization of shrubs. San

Diego: Academic Press, Inc. 656 p.

McKell, C. M.; Blaisdell, J. P.; Goodin, J. R., tech. eds. 1972.

Wildland shrubs—their biology and utilization: an international

symposium; 1971 July 12–16; Logan, UT. Gen. Tech. Rep. INT-1.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Forest and Range Experiment Station. 494 p.

Meyer, S. E.; Nelson, D. L.; Clement, S. 2001. Evidence for resistance polymorphism in the Bromus tectorum—Ustilago bullata

pathosystem: implications for biocontrol. Canadian Journal of

Plant Pathology. 23: 1–9.

Monsen, S. B.; Stevens, R., comps. [In review]. Restoring Western

ranges and wildlands. [Publisher not determined].

Moore, W. S. 1977. An evaluation of narrow hybrid zones in vertebrates. Quarterly Review of Biology. 52: 263–277.

Mozingo, H. N. 1987. Shrubs of the Great Basin, a natural history.

Reno: University of Nevada Press. 342 p.

Pendleton, R. L.; Kitchen, S. G.; McArthur, E. D. 1993. Origin of the

flax cultivar ‘APPAR’ and its taxonomic relationship to North

American and European perennial blue flax. In: Abstracts, eighth

wildland shrub symposium, arid land restoration; 1993 October

19–23; Las Vegas, NV. Provo, UT: Shrub Research Consortium: 23.

Plummer, A. P. 1972. Selection. In: McKell, C. M.; Blaisdell, J. P.;

Goodin, J. R., tech. eds. Wildland shrubs—their biology and

utilization: an international symposium; 1971 July 12–16; Logan, UT. Gen. Tech. Rep. INT-1. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Forest and Range

Experiment Station: 121–126.

Plummer, A. P.; Christensen, D. R.; Monsen, S. B. 1968. Restoring

big game range in Utah. Pub. 68-3. Salt Lake City, UT: Utah

Division of Fish and Game. 183 p.

Scholl, J. P.; Kelsey, R. G.; Shafizadeh, F. 1977. Involvement of

volatile compounds of Artemisia in browse preference by mule

deer. Biochemical Systematics and Ecology. 5: 291–295.

Stanton, D. J.; McArthur, E. D.; Freeman, D. C.; Golenberg, E. M.

2001. No genetic substructuring in Artemisia subgenus Tridentatae despite strong ecotypic subspecies selection. Biochemical Systematics and Ecology. 29.

Stevens, R.; McArthur, E. D. 1974. A simple field technique for

identification of some sagebrush taxa. Journal of Range Management. 27: 325–326.

Stutz, H. C., ed. 1976. Proceedings, symposium and workshop on the

occasion of the dedication of the U.S. Forest Service Shrub

Sciences Laboratory; 1975 November 4–6; Provo, UT. Provo, UT:

Brigham Young University, College of Biology and Agriculture.

168 p.

Stutz, H. C. 1978. Explosive evolution of perennial Atriplex in

Western America. Great Basin Naturalist Memoirs. 2: 161–169.

Stutz, H. C.; Melby, J. M.; Livingston, G. K. 1975. Evolutionary

studies of Atriplex: a relic gigas diploid population of Atriplex

canescens. American Journal of Botany. 62: 236–245.

Stutz, H. C.; Sanderson, S. C. 1979. The role of polyploidy in the

evolution of Atriplex canescens. In: Goodin, J. R.; Northington, D. K.,

eds. Arid land plant resources. Lubbock: Texas Tech University,

International Center for Arid and Semiarid Land Studies: 615–621.

Stutz, H. C.; Thomas, L. K. 1964. Hybridization and introgression

in Cowania and Purshia. Evolution. 18: 183–195.
16 USDA Forest Service Proceedings RMRS-P-21. 2001

McArthur The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective

Trimble, S. 1989. The sagebrush ocean, natural history of the Great

Basin. Reno: University of Nevada Press. 248 p.

Welch, B. L. [In review]. Big sagebrush: a sea fragmented into lakes,

puddles, and ponds. Gen. Tech. Rep. Fort Collins, CO: U.S.

Department of Agriculture, Forest Service, Rocky Mountain

Research Station.

Young, S. A. 1995. Verification of germplasm origin and genetic

status by seed certification agencies. In: Roundy, B. A.; McArthur,

E. D.; Haley, J. S.; Mann, D. K., comps. Proceedings: wildland

shrub and arid land restoration symposium; 1993 October 19–21;

Las Vegas, NV. Gen. Tech. Rep. INT-GTR-315. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Research Station: 292–295.

Appendix A: Publications of the

Shrub Sciences Laboratory,

1975 to 2000 ____________________

Publications included here are those of Shrub Sciences

Laboratory personnel, work funded or otherwise substantially furthered by Shrub Sciences Laboratory resources,

including work performed at the attached experimental

ranges (Benmore, Desert, and Great Basin) and personnel

working at those units.

1975

Barker, P. A. 1975. Ordinance control of street trees. Journal of

Arboriculture. 1: 212–216.

Blauer, A. C.; Plummer, A. P.; McArthur, E. D.; Stevens, R.; Guinta,

B. C. 1975. Characteristics and hybridization of important Intermountain shrubs. I. Rose family. Res. Pap. INT-169. Ogden, UT:

U.S. Department of Agriculture, Forest Service, Intermountain

Forest and Range Experiment Station. 36 p.

Ferguson, R. B.; Ryker, R. A.; Ballard, E. D. 1975. Portable oscilloscope technique for detecting dormancy in nursery stock. Gen.

Tech. Rep. INT-26. Ogden, UT: U.S. Department of Agriculture,

Forest Service, Intermountain Forest and Range Experiment

Station. 16 p.

Frischknecht, N. C. 1975. Native faunal relationships within the

pinyon-juniper ecosystem. In: Gifford, G. F; Busby, F. E., eds. The

pinyon-juniper ecosystem: a symposium; 1975 May 1–2; Logan,

UT. Logan: Utah State University and Utah Agricultural Experiment Station: 55–65.

Giunta, B. C.; Christensen, D. R.; Monsen, S. B. 1975. Interseeding

shrubs in cheatgrass with a browse seeder-scalper. Journal of

Range Management. 28: 398–402.

Hanks, D. L.; McArthur, E. D.; Plummer, A. P.; Giunta, B. C.;

Blauer, A. C. 1975. Chromatographic recognition of some palatable and unpalatable subspecies of rubber rabbitbrush in and

around Utah. Journal of Range Management. 28: 144–148.

Holmgren, R. C. 1975. The Desert Experimental Range. In: Hyder, D.

N., ed. Arid shrublands, proceedings of the third workshop of the

United States/Australia rangelands panel; 1973 March 26–April 5;

Tucson, AZ. Denver, CO: Society for Range Management: 18–22.

Martin, N. E.; Welch, B. L. 1975. Single dimension, multiple development thin-layer chromatography of sugars for densitometric

quantification. Res. Note INT-192. Ogden, UT: U.S. Department

of Agriculture, Forest Service, Intermountain Forest and Range

Experiment Station. 7 p.

Monsen, S. B. 1975. Selecting plants to rehabilitate disturbed areas.

In: Campbell, R. S.; Herbel, C. H., eds. Improved range plants.

Denver, CO: Society for Range Management: 76–90.

Shandruk, L. J. 1975. A comparison of three methods used to

analyze pronghorn antelope diets. Logan: Utah State University.

109 p. Thesis.

Stevens, R.; Giunta, B. C.; Plummer, A. P. 1975. Some aspects in the

biological control of juniper and pinyon. In: Gifford, G. F; Busby,

F. E., eds. The pinyon-juniper ecosystem: a symposium; 1975 May

1–2; Logan, UT. Logan: Utah State University and Utah Agricultural Experiment Station: 77–81.

Van Epps, G. 1975. Winter injury to fourwing saltbush. Journal of

Range Management. 28: 157–159.

Welch, B. L.; Martin, N. E. 1975a. Effects of Cronartium ribicola on

soluble sugars in Pinus monticoloa bark. Phytopathology. 65:

1025–1026.

Welch, B. L.; Martin, N. E. 1975b. Light and transmission microscopy

of white pine blister rust canker. Phytopathology. 65: 681-685.

1976

Anderson, D. C. 1976. The cyptogamic flora of desert soil crusts in

southern Utah. Provo, UT: Brigham Young University. 47 p. Thesis.

Anderson, D. C.; Rushforth, S. R. 1976. The cryptogam flora of

desert soil crusts in southern Utah, U.S.A. Nova Hedwigia. 28:

691–721.

Blauer, A. C.; Plummer, A. P.; McArthur, E. D.; Stevens, R.; Guinta,

B. C. 1976. Characteristics and hybridization of important Intermountain shrubs. II. Chenopod family. Res. Pap. INT-177. Ogden,

UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station. 42 p.

Davis, J. N. 1976. Ecological investigations in Cercocarpus ledifolius

Nutt. communites of Utah. Provo, UT: Brigham Young University. 56 p. Thesis.

Green, J. S. 1976. Influence of a dry wash habitat on distribution

and movement of heteromyid rodents. Provo, UT: Brigham Young

University. 27 p. Thesis.

Monsen, S. B.; Christensen, D. R. 1976. Woody plants for rehabilitating rangelands in the Intermountain region. In: Stutz, H. C.,

ed. Proceedings: symposium and workshop; 1975 November 6;

Provo, UT. Provo: Brigham Young University, College of Biology

and Agriculture: 72–119.

Plummer, A. P. 1976. Shrubs for the subalpine zone of the Wasatch

Plateau. In: Zuck, R. H.; Brown, L. F., eds. Proceedings of high

altitude revegetation workshop number 2. Fort Collins: Colorado

State University: 33–40.

Pope, C. L. 1976. A phylogenetic study of the suffrutescent shrubs

in the genus Atriplex. Provo, UT: Brigham Young University.

277 p. Dissertation.

Vickery, R. K., Jr.; Eldredge, F. A.; McArthur, E. D. 1976. Cytogenetic patterns of evolutionary divergence in the Mimulus glabratus

complex. American Midland Naturalist. 95: 377–389.

1977

Barker, P. A. 1977. A colorful mountaineer. Mountainwest. 3(4):

22, 25.

Barker, P. A. 1977. Planting strips in street rights-of-way: a key

public land resource. In: Andresen, J. W., ed. Trees and forests for

human settlements. Toronto, Ontario: University of Toronto

Press: 263–274.

Deacon, J. M. 1977. Partitioning of space and time by the western

jumping mouse, Zapus princeps utahensis Hall. Provo, UT:

Brigham Young University. 24 p. Thesis.

Freeman, D. C. 1977. Plant dioecy: ecology, evolution, and sex reversal.

Provo, UT: Brigham Young University. 58 p. Dissertation.

McArthur, E. D. 1977. Environmental induced changes of sex

expression in Atriplex canescens. Heredity. 38: 97–103.

McArthur, E. D.; Pope, C. L. 1977. Compositae. In: Löve, A. IOPB

chromosome number reports. L. V. Taxon. 26: 107–109.

McArthur, L. B. 1977. Utilization of nest boxes by birds in three

vegetational communities with special reference to the American

kestrel (Falco sparverius). Provo, UT: Brigham Young University. 44 p. Thesis.

Plummer, A. P. 1977. Revegetation of disturbed Intermountain area

sites. In: Thames, J. L., ed. Reclamation and use of disturbed land

in the Southwest. Tucson: University of Arizona Press: 302–339.

Plummer, A. P.; Monsen, S. B. 1977. Backpack seed collection. In:

31st annual report, vegetative rehabilitation and equipment

workshop; 1977 February 13–14; Portland, OR. Washington. DC:

U.S. Government Printing Office: 9–14.

Plummer, A. P.; Monsen, S. B.; Stevens, R. 1977. Intermountain

range plant names and symbols. Gen. Tech. Rep. INT-38. Ogden,

UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station. 82 p.
USDA Forest Service Proceedings RMRS-P-21. 2001 17

The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective McArthur

Pope, C. L.; McArthur, E. D. Chenopodiaceae. In: Löve, A. IOPB

chromosome number reports. L. V. Taxon. 26: 107–109.

Shepard, D. 1977. Prediction of sagebrush/grass biomass from

growth ring analysis. Reno: University of Nevada—Reno. 52 p.

Thesis.

Stevens, R.; Giunta, B. C.; Jorgensen, K. R.; Plummer, A. P. 1977.

Winterfat (Ceratoides lanata). Publ. 77-2. Salt Lake City: Utah

Division of Wildlife Resources. 41 p.

Welch, B. L.; Andrus, D. 1977. Rose hips—a possible high-energy

food for wintering mule deer. Res. Note INT-221. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station. 6 p.

1978

Anderson, D. C. 1978. Cryptogamic soil crusts: factors influencing

their development in Utah deserts and their recovery from

grazing on Utah winter ranges. Provo, UT: Brigham Young

University. 79 p. Dissertation.

Buchanan, B. B.; Harper, K. T.; Frischknecht, N. C. 1978. Allelopathic effects of bur buttercup tissue on germination and growth

of various grasses and forbs in vitro and in soil. Great Basin

Naturalist. 38: 90–96.

Everett, R. L.; Meeuwig, R. O.; Stevens, R. 1978. Deer mouse

preference for seed of commonly planted species, indigenous weed

species, and sacrifice foods. Journal of Range Management. 31:

70–73.

Frischknecht, N. C. 1978a. Effects of grazing, climate, fire, and

other disturbances on long-term productivity of sagebrush-grass

ranges. In: Hyder, D. N., ed. Proceedings of the First International Rangeland Congress; 1978 August 14–18; Denver, CO.

Denver: Society for Range Management: 633–635.

Frischknecht, N. C. 1978b. Use of shrubs for mined land reclamation

and wildlife habitat. In: Proceedings of workshop on reclamation

for wildlife habitat. Fort Collins, CO: Ecology Consultants: 1–14.

Giunta, B. C.; Stevens, R.; Jorgensen, K. R.; Plummer, A. P. 1978.

Antelope bitterbrush—an important wildland shrub. Publ. 78-

12. Salt Lake City: Utah Division of Wildlife Resources. 48 p.

Gutierrrez-G., J. S. 1978. Potential for cattle grazing on sheep range

in southwest Utah. Logan: Utah State University. 79 p. Thesis.

Norton, B. E. 1978. The impact of sheep grazing on long-term

successional trends in salt-desert shrub vegetation of southwestern Utah. In: Hyder, D. N., ed. Proceedings of the First International Rangeland Congress; 1978 August 14–18; Denver, CO:

Society for Range Management: 610–613.

McArthur, E. D.; Hanks, D. L.; Plummer, A. P.; Blauer, A. C.

1978a. Contributions to the taxonomy of Chrysothamnus

viscidiflorus (Astereae, Compositae) and other Chrysothamnus

species using paper chromatography. Journal of Range Management. 31: 216–223.

McArthur, E. D.; Plummer, A. P. 1978. Biogeography and management of native western shrubs: a case study, section Tridentatae

of Artemisia. Great Basin Naturalist Memoirs. 2: 229–243.

McArthur, E. D.; Plummer, A. P.; Davis, J. N. 1978b. Rehabilitation

of game range in the salt desert. In: Johnson, K. L., ed. Wyoming

shrublands: proceedings of the seventh Wyoming shrub ecology

workshop; 1978 May 31–June 1; Rock Springs, WY. Laramie:

University of Wyoming, Agricultural Extension Service: 23–50.

McArthur, E. D.; Plummer, A. P.; Van Epps, G. A.; Freeman, D. C.;

Jorgensen, K. R. 1978c. Producing fourwing saltbush in seed

orchards. In: Hyder, D. N., ed. Proceedings of the First International Rangeland Congress; 1978 August 14–18; Denver, CO.

Denver: Society for Range Management: 406–410.

Moden, W. L., Jr.; McKenzie, D. W.; Stevens, R. 1978. Interseeder

for rocky and brushy terrain, a progress report. ED&T Project No.

2582. San Dimas, CA: U.S. Department of Agriculture, Forest

Service, Equipment Development Center. 8 p.

Monsen, S. B. 1978. Report of field trials with the scarifier/seeder.

In: 32nd annual report, vegetative rehabilitation and equipment

workshop; 1978 February 5–6; San Antonio, TX. Washington,

DC: U.S. Government Printing Office: 17–19.

Monsen, S. B.; Plummer, A. P. 1978. Plants and treatment for

revegetation of disturbed sites in the Intermountain area. In:

Wright, R. A., ed. The reclamation of disturbed arid lands.

Albuquerque: University of New Mexico Press: 155–173.

Plummer, A. P.; Jorgensen, K. R. 1978. Harvesting, cleaning, and

storing seed of western shrubs. In: Nurseryman’s conference and

seed processing workshop; 1978 October; Eureka, CA. Eureka:

Western Forest Nursery Council and Intermountain

Nurseryman’s Association: D65–D76.

Stevens, R. 1978. Interseeder for rocky and brush areas. In: 32nd

annual report, vegetative rehabilitation and equipment workshop; 1978 February 5–6; San Antonio, TX. Washington. DC: U.S.

Government Printing Office: 6–10.

Tiedemann, A. R. 1978. Regional impacts of fire. In: Mooney, H. A.;

Bonnicksen, T. M.; Christensen, N. L., tech. coords. Proceedings

of the conference: fire regimes an ecosystem properties; 1978

December 11–15; Honolulu, HI. Gen. Tech. Rep. WO-26. Washington, DC: U.S. Department of Agriculture, Forest Service:

532–556.

Tiernan, C. F. 1978. The role of entomology in range management.

In: Hyder, D. N., ed. Proceedings of the First International

Rangeland Congress; 1978 August 14–18; Denver, CO. Denver:

Society for Range Management: 477–478.

Van Epps, G. A. 1978. Prototype seed harvester for fourwing

saltbush. In: 32nd annual report, vegetative rehabilitation and

equipment workshop; 1978 February 5–6; San Antonio, TX.

Washington, DC: U.S. Government Printing Office: 13–14.

Van Epps, G. A.; McKell, C. M. 1978. Major procedures for selecting

and establishing range shrubs as rehabilitators of disturbed

lands. In: Hyder, D. N., ed. Proceedings of the First International

Rangeland Congress; 1978 August 14–18; Denver, CO. Denver:

Society for Range Management: 352–354.

Vickery, R. K., Jr.; McArthur, E. D.; Purcell, S. P. 1978.

Scrophulariaceae. In: Löve, A. IOPB chromosome number reports. L. V. Taxon. 27: 223–231.

Welch, B. L. 1978. Relationships of soil salinity, ash, and crude

protein in Atriplex canescens. Journal of Range Management. 31:

132–133.

1979

Chambers, J. C. 1979. The effects of grazing on salt desert shrub

species survival during a period of below-average precipitation.

Logan, UT: Utah State University. 101 p. Thesis.

Clary, W. P. 1979. Variation in leaf anatomy and CO2 assimilation in

Sitanion hysterix ecotypes. Great Basin Naturalist. 39: 427–432.

Clary, W. P.; Kruse, W. H. 1979. Phenology and rate of height

growth of some forbs in the southwestern ponderosa pine type.

Res. Note RM-376. Fort Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky Mountain Forest and Range Experiment Station. 8 p.

Frischknecht, N. C. 1979. Biological methods: a tool for sagebrush

management. In: The sagebrush ecosystem: a symposium; 1978

April 27–28; Logan, UT. Logan: Utah State University, College of

Natural Resources: 121-128.

Frischknecht, N. C.; Ferguson, R. B. 1979. Revegetating processed

oil shale and coal spoils on semi-arid lands. EPA-600/7-79-068.

Cincinnati, OH: U.S. Environmental Protection Agency, Office of

Research and Development, Industrial Environmental Research

Laboratory. 47 p.

Jorgensen, K. R. 1979. Air amplifier seed collector. In: 33rd annual

report, vegetative rehabilitation and equipment workshop; 1979

February 11–12; Casper, WY. Washington, DC: U.S. Government

Printing Office: 17–18.

McArthur, E. D. 1979. Sagebrush systematics and evolution. In:

The sagebrush ecosystem: a symposium; 1978 April 27–28; Logan, UT. Logan: Utah State University, College of Natural

Resources: 14–22.

McArthur, E. D.; Blauer, A. C.; Plummer, A. P.; Stevens. R. 1979a.

Characteristics and hybridization of important Intermountain

shrubs. III. Sunflower family. Res. Pap. INT-220. Ogden, UT:

U.S. Department of Agriculture, Forest Service, Intermountain

Forest and Range Experiment Station. 82 p.

McArthur, E. D.; Pope, C. L. 1979. Karyotypes of four Artemisia

species: A. carruthii, A. filifolia, A. frigida, and A. spinescens.

Great Basin Naturalist. 39: 419–426.

McArthur, E. D.; Tiernan, C. F.; Welch, B. L. 1979b. Subspecies

specificity of gall forms on Chrysothamnus nauseosus. Great

Basin Naturalist. 39: 81–87.
18 USDA Forest Service Proceedings RMRS-P-21. 2001

McArthur The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective

Monsen, S. B. 1979a. Air amplifier seed collector trials. In: 33rd

annual report, vegetative rehabilitation and equipment workshop; 1979 February 11–12; Casper, WY. Washington, DC: U.S.

Government Printing Office: 18–20.

Monsen, S. B. 1979b. Rangeland interseeder field trials. In: 33rd

annual report, vegetative rehabilitation and equipment workshop; 1979 February 11–12; Casper, WY. Washington, DC: U.S.

Government Printing Office: 24–26.

Rinschede, G. 1979. Veränderung der Natürlichen Vegetation durch

Beweidung in den Westlichen U.S.A. (Change of natural vegetation by grazing in the western U.S.A.) Münster, Germany:

Universität Munster. 283 p. Dissertation.

Stevens, R. 1979a. Interseeder for rangelands. In: 33rd annual

report, vegetative rehabilitation and equipment workshop; 1979

February 11–12; Casper, WY. Washington, DC: U.S. Government

Printing Office: 22–24.

Stevens, R. 1979b. Tree transplanter for transplanting shrubs into

rangelands. In: 33rd annual report, vegetative rehabilitation and

equipment workshop; 1979 February 11–12; Casper, WY. Washington, DC: U.S. Government Printing Office: 26–29.

Stevens, R.; Moden, W. L., Jr. 1979. Interseeding and planting of

forbs and shrubs in desert regions. Paper 79-408. St. Joseph, MO:

American Society of Agricultural Engineers. 8 p.

Stutz, H. C.; Pope, C. L.; Sanderson, S. C. 1979. Evolutionary studies

of Atriplex: adaptative products from the natural hybrid, 6n A.

tridentata x 4n A. canescens. American Journal of Botany. 66:

1181–1193.

Welch, B. L.; McArthur, E. D. 1979a. Feasibility of improving big

sagebrush (Artemisia tridentata) for use on mule deer winter

ranges. In: Goodin, J. R.; Northington, D. K., eds. Arid land plant

resources. Lubbock, TX: Texas Tech University, International

Center for Arid and Semiarid Land Studies: 451–473.

Welch, B. L.; McArthur, E. D. 1979b. Variation in winter levels of

crude protein among Artemisia tridentata subspecies grown in a

uniform garden. Journal of Range Management. 32: 467–469.

West, N. E. 1979. Survival patterns of major perennials in salt

desert shrub communities of southwestern Utah. Journal of

Range Management. 32: 442–445.

1980

Cluff, L. K. 1980. Concentration of monoterpenoids in the rumen

ingesta of wild mule deer. Provo, UT: Brigham Young University.

16 p. Thesis.

Dewey, D. R.; Plummer, A. P. 1980. New collections of range plants

from the Soviet Union. Journal of Range Management. 33: 89–94.

Ferguson, R. B. 1980. Potting media for Atriplex production under

greenhouse conditions. Res. Note INT-301. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station. 7 p.

Harberd, D. J.; McArthur, E. D. 1980. Meiotic analysis of some

species and genus hybrids in the Brassiceae. In: Tsunoda, S;

Hinata, K.; Gomez-Campo, C., eds. Brassica crops and wild allies:

biology and breeding. Tokyo, Japan: Japan Scientific Societies

Press: 65–87.

Howard, C. G.; Jorgensen, K. R. 1980. ‘APPAR’ Lewis flax (Linum

lewisii, Pursh.) description, adaptation, use, culture, management, and seed production. Aberdeen, ID: U.S. Department of

Agriculture, Soil Conservation Service, Aberdeen Plant Materials Center. 6 p.

Jorgensen, C. D.; Smith, H. D.; Garcia, J. R. 1980. Temporal activity

patterns of a Dipodomys ordii population. Great Basin Naturalist. 40: 282–286.

Leonard, R. L. 1980. Electrophoresis of isoenzymes of 16 western

shrubs: technique development. Provo, UT: Brigham Young University. 30 p. Thesis.

McKenzie, D. W.; Stevens, R.; Moden, W. L., Jr. 1980. Development

of a rangeland interseeder for rocky or brushy terrain. Pap. 80-

1552. St. Joseph, MO: American Society of Agricultural Engineers. 7 p.

Medin, D. E.; Ferguson, R. E. 1980. A pilot planting trial on a

southwestern Idaho deer winter range. Res. Pap. INT-261. Ogden,

UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station. 13 p.

Smith, A. D.; Beale, D. M. 1980. Pronghorn antelope in Utah: some

research and observations. Publ. 80-13. Salt Lake City, UT: Utah

Division of Wildlife Resources. 88 p.

Tiedemann, A. R.; Lopushinsky, W.; Larsen, H. J., Jr. 1980. Plant

and soil responses to a commercial blue-green algae inoculant.

Soil Biology and Biochemistry. 12: 471–475.

Tiernan, C. 1980. Bugs are fun! Instructor. 89(8): 92-93.

Wagstaff, F. J. 1980. Impact of the 1975 Wallsburg fire on antelope

bitterbrush (Purshia tridentata). Great Basin Naturalist. 40:

299-302.

White, S. M. 1980. Interactions of pygmy rabbits and big sagebrush.

Provo, UT: Brigham Young University. 37 p. Thesis.

1981

Barker, J. R. 1981. Genetic differences between large and small

Artemisia tridentata plants in contiguous populations. Logan,

UT: Utah State University. 113 p. Dissertation.

Clary, W. P. 1981. Grazing, natural resource policy, and the biosphere reserves. In: Ffolliott, P. F; Halffter, G., tech. coords.

Proceedings: social and environmental consequences of natural

resources policies with special emphasis on biosphere reserves;

1980 April 8–13; Durango, Mexico. Gen. Tech. Rep. RM-88. Fort

Collins, CO: U.S. Department of Agriculture, Forest Service,

Rocky Mountain Forest and Range Experiment Station: 21–23.

Clary, W. P.; Holmgren, R. C. 1981. Observations of pronghorn

distribution in relation to sheep grazing on the Desert Experimental Range. In: Proceedings of the wildlife-livestock relationships symposium; 1981 April 20–22; Coeur d’Alene, ID. Moscow,

ID: University of Idaho Forest, Wildlife, and Range Experiment

Station: 581–592.

Clary, W. P.; Jameson, D. A. 1981. Herbage production following

tree and shrub removal in the pinyon-juniper type of Arizona.

Journal of Range Management. 34: 109–115.

Clary, W. P.; Jensen, C. E. 1981. Mathematical hypothesis for

herbage production potential on pinyon-juniper areas. Res. Pap.

INT-279. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Forest and Range Experiment Station. 8 p.

Everett, R. L.; Stevens, R. 1981. Deer mouse consumption of bitterbrush seed treated with four repellents. Journal of Range Management. 34: 393–396.

Ferguson, R. B.; Frischknecht, N. C. 1981. Shrub establishment on

reconstructed soils in semi-arid areas. In: Stelter, L. H.; DePuit,

E. J.; Mikol, S. A., tech. coords. Shrub establishment on disturbed

arid and semi-arid lands; 1980 December 2–3; Laramie, WY.

Cheyenne, WY: Wyoming Game and Fish Department: 57–63.

Freeman, D. C.; McArthur, E. D. 1981. A comparison of twig water

stress between males and females of six species of desert shrubs.

Forest Science. 28: 304–308.

Freeman, D. C.; McArthur, E. D.; Harper, K. T.; Blauer, A. C. 1981.

Influence of environment on the floral sex ratio of monoecious

plants. Evolution. 35: 194–197.

Frischknecht, N. C. 1981. Double-frequency sampling for inventorying vegetation on salt desert ranges. In: Arid land resource

inventories: developing cost efficient methods; 1980 November

30–December 6; La Paz, Mexico. Gen. Tech. Rep. WO-28. Washington, DC: U.S. Department of Agriculture, Forest Service:

435–440.

Goodrich, S. 1981. A floristic study of central Nevada. Provo, UT:

Brigham Young University. 400 p. Thesis.

Goodrich, S.; Neese, E; Peteron, J. S.; England, L. 1981. Vascular

plants of the Uinta Basin—a preliminary checklist. BLM-YAPT—040-4412. Salt Lake City, UT: U.S. Department of the

Interior, Bureau of Land Management, Utah State Office. 58 p.

Halffter, G.; Ffolliott, P. F.; Clary, W. P. 1981. Visits to Mapimi and

La Machila Biosphere Reserves. In: Ffolliott, P. F; Halffter, G.

tech. coords. Proceedings: social and environmental consequences

of natural resources policies with special emphasis on biosphere

reserves; 1980 April 8–13; Durango, Mexico. Gen. Tech. Rep. RM88. Fort Collins, CO: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Forest and Range Experiment Station:

52–53.

Harvey, S. J. 1981. Life history and reproductive strategies in

Artemisia. Bozeman, MT: Montana State University. 132 p.

Thesis.
USDA Forest Service Proceedings RMRS-P-21. 2001 19

The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective McArthur

Leonard, R. L.; McArthur, E. D.; Weber, D. J.; Wood, B. W. 1981.

Electrophoresis of isoenzymes of 16 western shrubs: technique

development. Great Basin Naturalist. 41: 377–389.

McArthur, E. D. 1981. Shrub selection and adaptation for rehabilitation plantings. In: Stelter, L. H.; DePuit, E. J.; Mikol, S. A., tech.

coords. Shrub establishment on disturbed arid and semi-arid

lands; 1980 December 2–3; Laramie, WY. Cheyenne, WY: Wyoming Game and Fish Department: 1–8.

McArthur, E. D.; Pope, C. L.; Freeman, D. C. 1981. Chromosomal

studies of subgenus Tridentatae of Artemisia: evidence for autopolyploidy. American Journal of Botany. 68: 589–605.

Nelson, D. L.; Krebill, R. G. 1981. A sagebrush wilt disease of

unknown cause. Great Basin Naturalist. 41: 184–191.

Pendleton, R. L. 1981. Sudies on the occurrence of vesiculararbuscular mycorrhizae: examination of natural and disturbed

communities of Utah and the Colorado Roan Plateau. Provo, UT:

Brigham Young University. 45 p. Thesis.

Robinove, C. J.; Chavez, P. S., Jr.; Gehring, D.; Holmgren, R. H.

1981. Arid land monitoring using landsat albedo difference images. Remote Sensing of Environment. 11: 133–156.

Stevens, R. 1981. Techniques for planting shrubs on wildland

disturbances. In: Stelter, L. H.; DePuit, E. J.; Mikol, S. A., tech.

coords. Shrub establishment on disturbed arid and semi-arid

lands; 1980 December 2–3; Laramie, WY. Cheyenne, WY: Wyoming Game and Fish Department: 26–36.

Stevens, R.; Jorgensen, K. R.; Davis, J. N. 1981a. Viability of seed

from thirty-two shrub and forb species through fifteen years of

warehouse storage. Great Basin Naturalist. 42: 274–277.

Stevens, R., Moden, W. L., Jr.; McKenzie, D. W. 1981b. Interseeding

and transplanting shrubs and forbs into grass communities.

Rangelands. 3: 55–58.

Tiedemann, A. R. 1981. Stream chemistry, nutrient economy, and

site productivity consequences wildland management and wildfire. In: Baumartner, D. M., ed. Proceedings of a symposium:

Interior West watershed management; 1981 April 8–10; Spokane, WA. Pullman, WA: Washington State University: 183–201.

Welch, B. L. 1981. Nutritive value of big sagebrush and other

shrubs. In: Stelter, L. H.; DePuit, E. J.; Mikol, S. A., tech. coords.

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December 2–3; Laramie, WY. Cheyenne, WY: Wyoming Game

and Fish Department: 9–22.

Welch, B. L.; McArthur, E. D. 1981. Variation of monoterpenoid

content among subspecies and accessions of Artemisia tridentata

grown in a uniform garden. Journal of Range Management. 34:

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Welch, B. L.; McArthur, E. D.; Davis, J. N. 1981. Differential preference of wintering mule deer for accessions of big sagebrush and for

black sagebrush. Journal of Range Management. 34: 409–411.

Welch, B. L.; Monsen, S. B. 1981. Winter crude protein among

accessions of fourwing saltbush grown in a uniform garden. Great

Basin Naturalist. 41: 343–346.

Welch, B. L.; Pederson, J. C. 1981. In vitro digestibility among

accessions of big sagebrush by wild mule deer and its relationship

to monoterpenoid content. Journal of Range Management. 34:

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Welsh, S. L.; Atwood, N. D.; Goodrich, S.; Neese, E.; Thorne, K. H.;

Albee, B. 1981. Preliminary index of Utah vascular plant names.

Great Basin Naturalist. 41: 1–108.

White, S. M.; Welch, B. L. 1981. Paired comparisons; a method for

ranking mule deer preference for various browse species. Res.

Note INT-308. Ogden, UT: U.S. Department of Agriculture,

Forest Service, Intermountain Forest and Range Experiment

Station. 4 p.

Woodward, R. A. 1981. An ecological consideration of the significance of cation exchange capacity of roots of some Utah range

plants. Provo, UT: Brigham Young University. 29 p. Thesis.

Young, J. A.; Evans, R. A.; Stevens, R.; Everett, R. L. 1981. Germination of Kochia prostrata seed. Agronomy Journal. 73: 957–961.

1982

Anderson, D. C.; Harper, K. T.; Holmgren, R. C. 1982a. Factors

influencing development of cryptogamic soil crusts in Utah deserts.

Journal of Range Management. 35: 180–185.

Anderson, D. C.; Harper, K. T.; Rushforth, S. R. 1982b. Recovery of

cryptogamic soil crusts from grazing on Utah winter ranges.

Journal of Range Management. 35: 355–359.

Blaisdell, J. P.; Murray, R. B.; McArthur, E. D. 1982. Managing

Intermountain rangelands—sagebrush-grass ranges. Gen. Tech.

Rep. INT-134. Ogden, UT: U.S. Department of Agriculture,

Forest Service, Intermountain Forest and Range Experiment

Station. 41 p.

Cedarleaf, J. D. 1982. Seasonal variation of monoterpenoids in big

sagebrush (Artemisia tridentata). Provo, UT: Brigham Young

University. 15 p. Thesis.

Clary, W. P.; Holmgren, R. C. 1982. Desert Experimental Range:

establishment and research contribution. Rangelands. 4: 261–264.

Cluff, L. K.; Welch, B. L.; Pederson, J. C.; Brotherson, J. D. 1981.

Concentration of monoterpenoids in the rumen ingesta of wild

mule deer. Journal of Range Management. 35: 192–194.

Freeman, D. C.; McArthur, E. D. 1982. A comparison of water stress

between males and females of four species of desert shrubs.

Forest Science. 28: 304–308.

Goodrich, S.; Lewis, M. F. 1982. Noteworthy collections: Carex

microglochin, C. parryana, Epilobium nevadense, and Kobresia

simpliciuscula. Madroño. 29: 57–61.

McArthur, E. D.; Freeman, D. C. 1982. Sex expression in Atriplex

canescens: genetics and environment. Botanical Gazette. 143:

476–482.

McArthur, E. D.; Hassell, W. G.; Stevens, R.; Davis, J. N.; Stranathan,

S. E.; Noller, G. L.; Tiedemann, A. R.; Goodrich, S. K. 1982. Notice

of naming and release of ‘Rincon’ fourwing saltbush (Atriplex

canescens) for wildlife and livestock range and disturbed land

reclamation. Washington, DC: U.S. Department of Agriculture,

Soil Conservation Service. 5 p.

McArthur, E. D.; Welch, B. L. 1982. Growth rate differences among

big sagebrush (Artemisia tridentata) accessions and subspecies.

Journal of Range Management. 35: 396–401.

Moore, T. B.; Stevens, R.; McArthur, E. D. 1982. Preliminary study

of some insects associated with rangeland shrubs with emphasis

on Kochia prostrata. Journal of Range Management. 35: 128–130.

Nelson, D. L. 1982. Phalacropsis dispar (Coleoptera: Palacridae) an

element in the natural control of native pine stem rust fungi in the

Western United States. Great Basin Naturalist. 42: 369–379.

Nelson, D. L.; Krebill, R. G. 1982. Occurrence and effect of

Chrusomyxa pirolata cone rust on Picea pungens in Utah. Great

Basin Naturalist. 42: 262–272.

Pederson, J. C.; Welch, B. L. 1982. Effects of monoterpenoid exposure on ability of rumen inocula to digest a set of forages. Journal

of Range Management. 35: 500–502.

Skousen, J. G. 1982. Evaluation of pinyon-juniper chainings for big

game in central Utah. Provo, UT: Brigham Young University. 74 p.

Thesis.

U.S. Department of Agriculture, Forest Service. 1982. Wildlife user

guide for mining and reclamation. Gen. Tech. Rep. INT-126.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Forest and Range Experiment Station. 77 p.

Welch, B. L.; Narjisse, H.; McArthur, E. D. 1982. Artemisia tridentata monoterpenoid effect on ruminant digestion and forage

selection. In: Margaris, N.; Koedam, A.; Volou, C., eds. Aromatic

plants: basic and applied aspects. The Hague, Netherlands:

Martinus Nijhoff Publishers: 73–86.

White, S. M.; Flinders, J. T.; Welch, B. L. 1982a. Preference of pygmy

rabbits, Brachylagus idahoensis, for various populations of big

sagebrush, Artemisia tridentata. Journal of Range Management.

35: 724–726.

White, S. M.; Welch, B. L.; Flinders, J. T. 1982b. Monoterpenoid

content of pygmy rabbit stomach ingesta. Journal of Range

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1983

Cedarleaf, J. D.; Welch, B. L.; Brotherson, J. D. 1983. Seasonal

variation of monoterpenoids in big sagebrush (Artemisia tridentata). Journal of Range Management. 36: 492–494.

Clark, R. A. 1983. The influence of environmental stress on male

and female functions in two dioecious shrubs of Utah. Provo, UT:

Brigham Young University. 31 p. Thesis.
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Clary, W. P. 1983a. Interfacing physical data and economics. In:

Wagstaff, F. J., comp. Proceedings—range economics symposium and workshop; 1982 August 31–September 2; Salt Lake

City, UT. Gen. Tech. Rep. INT-149. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and

Range Experiment Station: 115–119.

Clary, W. P. 1983b. Overstory-understory relationships: spruce-fir

forests. In: Overstory-understory relationships in western forests.

Western Regional Res. Publ. 1. Fort Collins, CO: Colorado State

University, Colorado Agricultural Experiment Station: 9–12.

Clary, W. P.; Beale, D. M. 1983. Pronghorn reactions to winter sheep

grazing, plant communities, and topography in the Great Basin.

Journal of Range Management. 36: 749–752.

Clary, W. P.; Johnson, T. J. 1983. Land imprinter results in Utah.

In: Vegetative rehabilitation and equipment workshop, 37th annual report; 1983 February 13–14; Albuquerque, NM. Missoula,

MT: U.S. Department of Agriculture, Forest Service, Equipment

Development Center: 23–24.

Davis, J. N. 1983. Performance comparison among populations of

bitterbrush, cliffrose, and bitterbrush-cliffrose crosses on study

sites throughout Utah. In: Tiedemann, A. R; Johnson, K. L.,

comps. Proceedings: research and management of bitterbrush

and cliffrose in Western North America; 1982 April 13–15; Salt

Lake City, UT. Gen. Tech. Rep. INT-152. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station: 38–44.

Ferguson, R. B. 1983. Use of rosaceous shrubs for wildland plantings in the Intermountain West. In: Monsen, S. B.; Shaw, N.,

comps. Managing Intermountain rangelands—improvement of

range and wildlife habitats: proceedings of a symposium; 1981

September 15–17; Twin Falls, ID; 1982 June 22–24; Elko, NV.

Gen. Tech. Rep. INT-157. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station: 136–149.

Ferguson, R. B.; Frischknecht, N. C. 1983. Revegetating processed

oil shale in the upper mountain brush zone of Colorado. Res. Pap.

INT-321. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Forest and Range Experiment Station. 9 p.

Ferguson, R. B.; Medin, D. E. 1983. Long-term changes in an

ungrazed bitterbrush plant community in southwest Idaho. In:

Tiedemann, A. R; Johnson, K. L., comps. Proceedings: research

and management of bitterbrush and cliffrose in Western North

America; 1982 April 13–15; Salt Lake City, UT. Gen. Tech. Rep.

INT-152. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Forest and Range Experiment Station:

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Ffolliott, P. F.; Clary, W. P. 1983. An annotated bibliography of

understory—overstory vegetation relationships. Gen. Tech. Rep.

INT-136. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Forest and Range Experiment Station.

39 p.

Frank, C. T. 1983. Photosynthesis and growth of different accessions

of big sagebrush. Provo, UT: Brigham Young University. 22 p.

Thesis.

Frischknecht, N. C. 1983. Plants adapted to summer rangelands. In:

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of a symposium; 1981 September 15–17; Twin Falls, ID; 1982

June 22–24; Elko, NV. Gen. Tech. Rep. INT-157. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station: 102-107.

Goodrich, S. 1983. Utah flora: Salicaceae. Great Basin Naturalist.

43: 531–550.

Goodrich, S.; Henderson, D.; Chokewa, A. 1983. Noteworthy collections—Idaho, Astragalus gilviflorus and Hackelia davisii.

Madroño. 39: 63.

Goodrich, S.; Welsh, S. L. 1983. New variety of Stephanomeria tenuifolia

(Compositae) from Utah. Great Basin Naturalist. 43: 375.

Grah, O. J. 1983. Spatial and temporal distribution of infiltration

rates on a small subalpine watershed. Logan, UT: Utah State

University. 172 p. Thesis.

McArthur, E. D. 1983a. Important shrubs for wildland plantings,

Compositae (Asteraceae). In: Monsen, S. B.; Shaw, N., comps.

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McArthur, E. D. 1983b. Taxonomy, origin, and distribution of big

sagebrush (Artemisia tridentata) and allies (subgenus

Tridentatae). In: Johnson, K. L., ed. Proceedings of the first

Utah shrub ecology workshop; 1981 September 9–10; Ephraim,

UT. Logan: Utah State University, College of Natural Resources: 3–13.

McArthur, E. D.; Hassell, W. D.; Stevens, R. 1983a. Naming and

release of ‘Rincon’ fourwing saltbush (Atriplex canescens) for

wildlife and livestock range and disturbed land reclamation.

Plant Release Notice. Salt Lake City, UT: U.S. Department of

Agriculture, Soil Conservation Service, Utah State Office. 5 p.

McArthur, E. D.; Stevens, R. 1983. Briefing paper on perennial

summer cypress. Tech. Notes, Plant Materials 44. Denver, CO:

U.S. Department of Agriculture, Soil Conservation Service. 2 p.

McArthur, E. D.; Stevens, R.; Blauer, A. C. 1983b. Growth performance comparisons among 18 accessions of fourwing saltbush

(Atriplex canescens) at two sites in central Utah. Journal of Range

Management. 36: 78–81.

McArthur, E. D.; Stutz, H. C.; Sanderson, S. C. 1983c. Taxonomy,

distribution, and cytogenetics of Purshia, Cowania, and Fallugia

(Rosoideae, Rosaceae). In: Tiedemann, A. R.; Johnson, K. L.,

comps. Proceedings: research and management of bitterbrush

and cliffrose in Western North America; 1982 April 13–15; Salt

Lake City, UT. Gen. Tech. Rep. INT-152. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station: 4–24.

Monsen, S. B. 1983. Plants for revegetation of riparian sites within

the Intermountain Region. In: Monsen, S. B.; Shaw, N., comps.

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wildlife habitats: proceedings of a symposium; 1981 September

15–17; Twin Falls, ID; 1982 June 22-24; Elko, NV. Gen. Tech. Rep.

INT-157. Ogden, UT: U.S. Department of Agriculture, Forest

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83–89.

Monsen, S. B.; Shaw, N. 1983a. Benefits of seeding legumes with

grasses on western phosphate mine disturbances. In: Robertson,

D. J., ed. Reclamation and the phosphate industry; 1983, January

26–28; Clearwater Beach, FL. Bartow, FL: Florida Institute of

Phosphate Research: 464–478.

Monsen, S. B.; Shaw, N., comps. 1983b. Managing Intermountain

rangelands—improvement of range and wildlife habitats: proceedings of a symposium; 1981 September 15–17; Twin Falls, ID;

1982 June 22–24; Elko, NV. Gen. Tech. Rep. INT-157. Ogden, UT:

U.S. Department of Agriculture, Forest Service, Intermountain

Forest and Range Experiment Station. 194 p.

Monsen, S. B.; Shaw, N. 1983c. Reynolds Creek species adaptability plantings. In: Volume II—comprehensive report ARS/BLM

cooperative studies: Reynolds Creek Watershed. Boise, ID: U.S.

Department of Agriculture, Agriculture Research Service, Northwest Watershed Research Center: 5-16–5-27.

Monsen, S. B.; Shaw, N. 1983d. Seeding antelope bitterbrush with

grasses on south-central Idaho rangelands—a 39-year response.

In: Tiedemann, A. R; Johnson, K. L., comps. Proceedings: research and management of bitterbrush and cliffrose in Western

North America; 1982 April 13–15; Salt Lake City, UT. Gen. Tech.

Rep. INT-152. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station: 116–136.

Nelson, D. L. l983. Occurrence and nature of actinorhizae on

Cowania stansburiana and other Rosaceae. In: Tiedemann, A. R;

Johnson, K. L., comps. Proceedings: research and management of

bitterbrush and cliffrose in Western North America; 1982 April

13–15; Salt Lake City, UT. Gen. Tech. Rep. INT-152. Ogden, UT:

U.S. Department of Agriculture, Forest Service, Intermountain

Forest and Range Experiment Station: 225–239.

Nelson, D. L.; Tiernan, C. F. 1983. Winter injury of sagebrush and

other wildland shrubs in the Western United States. Res. Pap.

INT-314. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Forest and Range Experiment Station.

17 p.

Pendleton, R. L.; Smith, B. N. 1983. Vesicular-arbuscular mycorrhizae of weedy and colonizer plant species at disturbed sites in

Utah. Oecologia. 59: 296–301.
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Ramsey, R. D. 1983. Influence of tree overstory on understory

production and composition in aspen forests of central Utah.

Provo, UT: Brigham Young University. 27 p. Thesis.

Shaw, N.; Monsen, S. B. 1983a. Non-leguminous forbs for rangeland

sites. In: Monsen, S. B.; Shaw, N., comps. Managing Intermountain rangelands—improvement of range and wildlife habitats:

proceedings of a symposium; 1981 September 15–17; Twin Falls,

ID; 1982 June 22–24; Elko, NV. Gen. Tech. Rep. INT-157. Ogden,

UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station: 123–131.

Shaw, N. L.; Monsen, S. B. 1983b. Phenology and growth habits of

nine antelope bitterbrush, desert bitterbrush, Stansbury cliffrose,

and Apache-plume accessions. In: Tiedemann, A. R; Johnson, K.

L., comps. Proceedings: research and management of bitterbrush

and cliffrose in Western North America; 1982 April 13–15; Salt

Lake City, UT. Gen. Tech. Rep. INT-152. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station: 55–69.

Stevens, R. 1983a. Selecting species mixtures for optimum habitat

development on disturbed land. In: Proceedings of the third

annual reclamation symposium, native plants; 1983 January 10–

11; Salt Lake City, UT. Salt Lake City, UT: Native Plants, Inc.:

42–57.

Stevens, R. 1983b. Species adapted for seeding: mountain brush,

big, black, and low sagebrush in pinyon-juniper communities. In:

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of a symposium; 1981 September 15–17; Twin Falls, ID; 1982

June 22–24; Elko, NV. Gen. Tech. Rep. INT-157. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station: 78–82.

Stevens, R.; Monsen, S. B.; Shaw, N.; McArthur, E. D.; James, G.;

Davis, G.; Jorgensen, K. R.; Davis, J. N. 1983a. Naming and

releasing of ‘Ephraim’ crested wheatgrass for commercial production and marketing of seed. Washington, DC: U.S. Department of

Agriculture, Soil Conservation Service. 2 p.

Stevens, R.; Monsen, S. B.; Shaw, N.; Welch, B.; James, G.; Jorgensen,

K. R.; Davis, J. N. 1983b. Naming and release of ‘Paiute’

orchardgrass for commercial production and marketing of seed.

Washington, DC: U.S. Department of Agriculture, Soil Conservation Service. 3 p.

Tiedemann, A. R. 1983. Response of bitterbrush and associated

plant species to broadcast nitrogen, phosphorus, and sulfur

fertilization. In: Tiedemann, A. R; Johnson, K. L., comps. Proceedings: research and management of bitterbrush and cliffrose

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Gen. Tech. Rep. INT-152. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station: 240–255.

Tiedemann, A. R.; Driver, C. H. 1983. Snow eriogonum, a native

half-shrub to revegetate winter game ranges. Reclamation and

Revegetation. 2: 31–39.

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and management of bitterbrush and cliffrose in Western North

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279 p.

Tiedemann, A. R.; Lopez, C. F. 1983. Soil nutrient assessment of

mine spoils. In: Aldon, E. F.; Oaks, W. R., eds. Reclamation of

mined lands in the Southwest: proceedings of symposium; 1982

October 20–22; Albuquerque, NM. Albuquerque: Soil Conservations Service of America, New Mexico Chapter: 66–79.

Wagstaff, F. J. 1983a. Economic incentives for managing quaking aspen in the Mountain West and evaluating proposed

improvements of public rangelands. Provo, UT: Brigham Young

University. 40 p. Dissertation.

Wagstaff, F. J. 1983b. Economics as a tool for natural rangeland

managers. Rangelands. 5: 121–122.

Wagstaff, F. J. 1983c. Evaluating proposed improvements of public

rangelands. Gen. Tech. Rep. INT-150. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and

Range Experiment Station. 4 p.

Wagstaff, F. J. 1983d. Externalities caused by multiple use on public

rangelands. In: Wagstaff, F. J., comp. Proceedings—range economics symposium and workshop; 1982 August 31–September 2;

Salt Lake City, UT. Gen. Tech. Rep. INT-149. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station: 82–85.

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City, UT. Gen. Tech. Rep. INT-149. Ogden, UT: U.S. Department

of Agriculture, Forest Service, Intermountain Forest and Range

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Welch, B. L. 1983a. Big sagebrush: nutrition, selection, and controversy. In: Johnson, K. L., ed. Proceedings of the first Utah shrub

ecology workshop; 1981 September 9–10; Ephraim, UT. Logan,

UT: Utah State University, College of Natural Resources: 21–33.

Welch, B. L. 1983b. Improving the nutritive value of winter range

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Welch, B. L.; McArthur, E. D. 1983. Briefing paper on sagebrush

values. Tech. Notes, Plant Materials 45. Denver, CO: U.S. Department of Agriculture, Soil Conservation Service. 2 p.

Welch, B. L.; McArthur, E. D.; Davis, J. N. 1983a. Mule deer

preference and monoterpenoids (essential oils). Journal of Range

Management. 36: 485–487.

Welch, B. L.; Monsen, S. B.; Shaw, N. L. 1983b. Nutritive value of

antelope and desert bitterbrush, Stansbury cliffrose, and Apacheplume. In: Tiedemann, A. R; Johnson, K. L., comps. Proceedings:

research and management of bitterbrush and cliffrose in Western

North America; 1982 April 13–15; Salt Lake City, UT. Gen. Tech. Rep.

INT-152. Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Forest and Range Experiment Station: 173–185.

Welch, B. L.; Pederson, J. C.; Clary, W. P. 1983c. Ability of different

rumen inocula to digest a set of range forages. Journal of Wildlife

Management. 47: 873–877.

1984

Astroth, K. A.; Frischknecht, N. C. 1984. Managing Intermountain

rangelands—research on the Benmore Experimental Range, 1940–

1984. Gen. Tech. Rep. INT-175. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Forest and Range

Experiment Station. 44 p.

Atwood, N. D.; Goodrich, S.; Welsh, S. L. 1984. New Astragalus

(Leguminosae) from Goose Creek drainage, Utah-Nevada. Great

Basin Naturalist. 44: 263–264.

Blaisdell, J. P.; Holmgren, R. C. 1984. Managing Intermountain

rangelands—salt-desert shrub ranges. Gen. Tech. Rep. INT-163.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Forest and Range Experiment Station. 52 p.

Bowden, D. C.; Anderson, A. E.; Medin, D. E. 1984. Sampling plans

for mule deer sex and age ratios. Journal of Wildlife Management.

48: 500–509.

Clary, W. P.; Tiedemann, A. R. 1984. Development of ‘Rincon’

fourwing saltbush, winterfat and other shrubs form seed following fire. In: Tiedemann, A. R.; McArthur, E. D.; Stutz, H. C.;

Stevens, R.; Johnson, K. L., comps. Proceedings—symposium on

the biology of Atriplex and related chenopods; 1983 May 2–6;

Provo, UT. Gen. Tech. Rep. INT-172. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and

Range Experiment Station: 273–280.

Davis, J. N.; Welch, B. L. 1984. Seasonal variation in crude protein

of Kochia prostrata. In: Tiedemann, A. R.; McArthur, E. D.;

Stutz, H. C.; Stevens, R.; Johnson, K. L., comps. Proceedings—

symposium on the biology of Atriplex and related chenopods;

1983 May 2–6; Provo, UT. Gen. Tech. Rep. INT-172. Ogden, UT:

U.S. Department of Agriculture, Forest Service, Intermountain

Forest and Range Experiment Station: 145–149.

Freeman, D. C.; McArthur, E. D. 1984. The relative influences of

mortality, non-flowering, and sex change on the sex ratios of six

Atriplex species. Botanical Gazette. 145: 385–394.

Freeman, D. C.; McArthur, E. D.; Harper, K. T. 1984. The adaptative

significance of sexual lability in plants using Atriplex canescens

as the principal example. Annals of the Missouri Botanical

Garden. 71: 265–277.
22 USDA Forest Service Proceedings RMRS-P-21. 2001

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Frischknecht, N. C.; Ferguson, R. B. 1984. Performance of

Chenopodiaceae species on processed oil shale. In: Tiedemann,

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comps. Proceedings—symposium on the biology of Atriplex and

related chenopods; 1983 May 2–6; Provo, UT. Gen. Tech. Rep.

INT-172. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Forest and Range Experiment Station:

293–297.

Goodrich, S. 1984. Checklist of vascular plants of the Canyon and

Church Mountains. Great Basin Naturalist. 44: 277–295.

Harniss, R. O.; Nelson, D. L. 1984. A severe epidemic of Marssonina

leaf blight on quaking aspen in northern Utah. Res. Note INT339. Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Forest and Range Experiment Station. 6 p.

Holmgren, R. C. 1984. The Great Basin cold desert: some physical

geography. In: Tiedemann, A. R.; McArthur, E. D.; Stutz, H. C.;

Stevens, R.; Johnson, K. L., comps. Proceedings—symposium on

the biology of Atriplex and related chenopods; 1983 May 2–6;

Provo, UT. Gen. Tech. Rep. INT-172. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and

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Jorgensen, K. R.; Davis, J. N. 1984. A technique of retaining seed

viability in Kochia prostrata ([L.] Schrad. In: Tiedemann, A. R.;

McArthur, E. D.; Stutz, H. C.; Stevens, R.; Johnson, K. L., comps.

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McArthur, E. D. 1984. Natural diversity of western range shrubs.

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McArthur, E. D.; Blauer, A. C.; Noller, G. L. 1984a. Propagation of

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McArthur, E. D.; Sanderson, S. C. 1984. Distribution, systematics,

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McArthur, E. D.; Stranathan, S. E.; Noller, G. L. 1984b. ‘Rincon’

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Medin, D. E. 1984. Breeding birds of an ancient bristlecone pine stand

in east central Nevada. Great Basin Naturalist. 44: 272–276.

Monsen, S. B. 1984. Use of shrubs on mine spoils. In: Murphy, P. M.,

comp. The challenge of producing native plants for the Intermountain area: proceedings, Intermountain Nurseryman’s Association 1983 conference; 1983 August 8–11; Las Vegas, NV. Gen.

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Monsen, S. B.; Richardson, B. Z. 1984. Seeding shrubs with herbs

on a semiarid mine site with and without topsoil. In: Tiedemann, A. R.; McArthur, E. D.; Stutz, H. C.; Stevens, R.; Johnson,

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Moore, T. B.; Stevens, R. 1984. Distribution and importance of the

Atriplex case-bearing moth, Coleophora atriplicivora Cockerel,

on some chenopod shrubs, especially Atriplex canescens (Pursh.)

Nutt. In: Tiedemann, A. R.; McArthur, E. D.; Stutz, H. C.;

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Nelson, D. L. 1984. Toward producing disease-free container grown

native wildland plants. In: Murphy, P. M., comp. The challenge of

producing native plants for the Intermountain area: proceedings,

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Nelson, D. L.; Schuttler. P. L. 1984. Histology of Cowania

stansburiana actinorhizae. Northwest Science. 58: 49–56.

Noller, G. L.; Stranathan, S. E.; McArthur, E. D. 1984. Establishment and initial results from a ‘Rincon’ fourwing saltbush seed

orchard. In: Tiedemann, A. R.; McArthur, E. D.; Stutz, H. C.;

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Range Experiment Station: 196–204.

Pederson, J. D. 1984. Factors influencing nutrition, productivity,

and mortality of mule deer in Utah. Provo, UT: Brigham Young

University. 33 p. Dissertation.

Platts, W. S.; Wagstaff, F. J. 1984. Fencing to control livestock grazing

on riparian habitats along streams; is it a viable alternative? North

American Journal of Fisheries Management. 4: 266–272.

Roos, R. C. 1984. Heritable variation in Sarcobatus vermiculaatus.

Provo, UT: Brigham Young University. 41 p. Thesis.

Sanderson, S. C.; Goodrich, S.; McArthur, E. D. 1984. Asteraceae,

Chenopodiaceae, Fagaceae. In: Löve, A. IOPB chromosome number reports. LXXXV. Taxon. 33: 756–760.

Sanderson, S. C.; Stutz, H. C. 1984. Flavonoid aglycones of diploid

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Shaw, N.; Monsen, S. B. 1984. Nursery propagation and outplanting of bareroot chenopod seedlings. In: Tiedemann, A. R.;

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251–260.

Shaw, N. L.; Monsen, S. B.; Carlson, J. R. 1984. Notice of release of

‘Lassen’ antelope bitterbrush. Salt Lake City, UT: U.S. Department of Agriculture, Soil Conservation Service. 4 p.

Stevens, R.; Jorgensen, K. R.; McArthur, E. D.; Davis, J. N. 1984.

Notice of release of ‘Immigrant’ forage kochia. Salt Lake City, UT:

U.S. Department of Agriculture, Soil Conservation Service. 3 p.

Stevens, R.; Van Epps, G. A. Seeding techniques to improve establishment of forage kochia and fourwing saltbush. In: Tiedemann,

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Stutz, H. C.; Sanderson, S. C. 1984. Evolutionary studies of Atriplex:

chromosome races of Atriplex confertifolia (shadscale). American

Journal of Botany. 70: 1536–1547.

Tiedemann, A. R. 1984. Shrub Research Consortium formed. Great

Basin Naturalist. 44: 182.

Tiedemann, A. R.; McArthur, E. D.; Lopez, C. F. 1984a. Carbohydrate and nitrogen concentrations in leaves of three shrub

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UT. Gen. Tech. Rep. INT-172. Ogden, UT: U.S. Department of

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Wagstaff, F. J. 1984. Economic considerations in use and management of Gambel oak for fuelwood. Gen. Tech. Rep. INT-165.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Forest and Range Experiment Station. 8 p.

Welch, B. L.; Davis, J. N. 1984. In vitro digestibility of Kochia

prostrata (L.) Schrad. Great Basin Naturalist. 44: 296–298.

Welch, B. L.; Monsen, S. B. 1984. Winter nutritive value of accessions of fourwing saltbush (Atriplex canescens) grown on a uniform garden. In: Tiedemann, A. R.; McArthur, E. D.; Stutz, H. C.;

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Provo, UT. Gen. Tech. Rep. INT-172. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and

Range Experiment Station: 138–144.

Woodward, R. D.; Harper, K. T.; Tiedemann, A. R. 1984. An ecological consideration of the significance of cation-exchange capacity

of roots of some Utah range plants. Plant and Soil. 79: 169–180.

1985

Behan, B.; Welch, B. L. 1985. Black sagebrush: mule deer winter

preference and monoterpenoid content. Journal of Range Management. 38: 278–280.

Bunderson, E. D.; Weber, D. J.; Davis, J. N. 1985. Soil mineral

composition and nutrient uptake in Juniperus osteosperma in 17

Utah sites. Soil Science. 139: 139–148.

Carlson, J. R.; McArthur, E. D., eds. 1985. Proceedings: selected

papers presented at the 38th annual meeting of the Society for

Range Management, range plant improvements in Western North

America; 1985 February 14; Salt Lake City, UT. Denver, CO:

Society for Range Management: 107–220.

Clary, W. P.; Beale, D. M.; Holmgren, R. C. 1985a. Melanistic

pronghorn fawns on the Desert Experimental Range. Southwestern Naturalist. 30: 159–162.

Clary, W. P.; Goodrich, S.; Smith, B. M. 1985b. Response of broom

snakeweed to application of tebuthiuron. Res. Note INT-350.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Forest and Range Experiment Station. 4 p.

Clary, W. P.; Goodrich, S.; Smith, B. M. 1985c. Response of Gambel

oak to tebuthiuron in central Utah. Res. Note INT-351. Ogden,

UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station. 4 p.

Clary, W. P.; Goodrich, S.; Smith, B. M. 1985d. Response to

tebuthiuron by Utah juniper and mountain big sagebrush communities. Journal of Range Management. 38: 56–60.

Clary, W. P.; Tiedemann, A. R. 1985. Biomass distribution in

northcentral Utah Gambel oak stands. In: Johnson, K. L., ed.

Proceedings of the third Utah shrub ecology workshop; 1983

August 30–31; Provo, UT. Logan: Utah State University, College

of Natural Resources: 9–12.

Davis, J. N.; Welch, B. L. 1985. Winter preference, nutritive value,

and other range use characteristics of Kochia prostrata (L.)

Schrad. Great Basin Naturalist. 45: 778–783.

Ferguson, R. B.; Frischknecht, N. C. 1985. Reclamation on Utah’s

Emery and Alton coal fields: techniques and plant materials. Res.

Pap. INT-335. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Forest and Range Experiment Station. 78 p.

Goodrich, S. 1985. Utah flora: Saxifragaceae. Great Basin Naturalist. 45: 155–172.

Goodrich, S.; Atwood, D.; Neese, E. 1985a. Noteworthy collections:

Utah. Madroño. 32: 125.

Goodrich, S.; McArthur, E. D.; Winward, A. H. 1985b. A new

combination and a new variety in Artemisia tridentata. Great

Basin Naturalist. 45: 155–172.

Harper, K. T.; Wagstaff, F. J.; Kunzler, L. M. 1985. Biology and

management of the Gambel oak vegetative types: a literature

review. Gen. Tech. Rep. INT-179. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Forest and Range

Experiment Station. 31 p.

Hess, W. M.; Nelson, D. L.; Sturges, D. L. 1985. Morphology and

ultrastructure of a snowmold fungus on sagebrush (Artemisia

tridentata). Mycologia. 77: 637–647.

Masslich, W. J. 1985. Aspen-beaver relationships in the Strawberry

Valley of central Utah. Provo, UT: Brigham Young University. 38 p.

Thesis.

McArthur, E. D.; Sanderson, S. C. 1985. A cytotaxonomic contribution to the western North American rosaceous flora. Madroño. 32:

24–28.

McArthur, E. D.; Welch, B. L.; Nelson, D. L. 1985. Developing

improved cultivars of sagebrushes and other composite shrubs.

In: Carlson, J. R.; McArthur, E. D., eds. Proceedings: selected

papers presented at the 38th annual meeting of the Society for

Range Management, range plant improvements in Western North

America; 1985 February 14; Salt Lake City, UT. Denver, CO:

Society for Range Management: 188–196.

Monsen, S. B.; Davis, J. N. 1985. Progress in the improvement of

selected western North American rosaceous shrubs. In: Carlson,

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Management, range plant improvements in Western North

America; 1985 February 14; Salt Lake City, UT. Denver, CO:

Society for Range Management: 201–209.

Monsen, S. B.; McArthur, E. D. 1985. Factors influencing establishment of seeded broadleaf herbs and shrubs following fire. In:

Sanders, K.; Durham, J., eds. Rangelands fire effects symposium; 1984 November 27–29; Boise, ID. Boise: U.S. Department

of the Interior, Bureau of Land Management, Idaho State Office:

112–124.

Monsen, S. B.; Stevens, R. 1985. ‘Paiute’ orchardgrass—forage

species for semiarid range and wildland sites. Rangelands. 7:

114–115.

Monsen, S. B.; Stevens, R.; James, G.; Jorgensen, K. R.; Oaks,

W. R. 1985a. Naming and release of ‘Hatch’ winterfat for

commercial production and marketing of seed and seedlings.

Washington, DC: U.S. Department of Agriculture, Soil Conservation Service. 7 p.

Monsen, S. B.; Stevens, R.; Jorgensen, K. R. 1985b. Seed harvesters—an evaluation of existing machines and projected needs. In:

39th annual report, vegetative rehabilitation and equipment

workshop; 1985 February 10–11; Salt Lake City, UT. Missoula ,

MT: U.S. Department of Agriculture, Forest Service, Equipment

Development Center: 37–39.

Nielsen, D. B.; Lytle, D. D.; Wagstaff, F. 1985. Who gains (or loses)

when big-game uses private lands. Utah Science. 46(2): 48–51.

O’Neal, G. T. 1985. Behavioral ecology of the Nevada kit fox (Vulpes

macrotis nevadensis) on a managed desert rangeland. Provo, UT:

Brigham Young University. 75 p. Thesis.

Pederson, J. C.; Welch, B. L. 1985. Comparison of ponderosa pine as

feed and nonfeed trees for Abert squirrels. Journal of Chemical

Ecology. 11: 149–157.

Pendleton, R. L.; Sanderson, S. C.; McArthur, E. D. 1985. Morphologic and enzymatic variability among Gambel oak clones in

north-central Utah. In: Johnson, K. L., ed. Proceedings of the

third Utah shrub ecology workshop; 1983 August 30–31; Provo,

UT. Logan, UT: Utah State University, College of Natural Resources: 19–28.

Stevens, R. 1985a. Depth of interseeding scalps can affect growth of

seeded mountain big sagebrush. In: 39th annual report, vegetative rehabilitation and equipment workshop; 1979 February 10–

11; Salt Lake City, UT. Missoula, MT: U.S. Department of

Agriculture, Forest Service, Equipment Development Center:

25–27.

Stevens, R. 1985b. Interseeding with a modified Sieco Fireplow can

result in increased seedling numbers. In: 39th annual report,

vegetative rehabilitation and equipment workshop; 1979 February 10–11; Salt Lake City, UT. Missoula, MT: U.S. Department

of Agriculture, Forest Service, Equipment Development Center:

22–24.

Stevens, R. 1985c. Ten commandments of range restoration. In:

Proceedings—Cedar Valley conservation; 1985 January 21; Cedar Valley, UT. Logan: Utah State University Extension Service:

14–15.

Stevens, R.; Davis, J. N. 1985. Opportunities for improving forage

production in the Gambel oak types of Utah. In: Johnson, K. L.,

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Stevens, R.; Jorgensen, K. R.; McArthur, E. D.; Davis, J. N. 1985a.

‘Immigrant’ forage kochia. Rangelands. 7: 22–23.

Stevens, R.; Monsen, S. B. 1985a. ‘Ephraim’ crested wheatgrass—

a rhizomatous grass. Rangelands. 7: 163–164.

Stevens, R.; Monsen, S. B. 1985b. Recent plant releases for western

wildlands. In: 39th annual report, vegetative rehabilitation and

equipment workshop; 1985 February 10–11; Salt Lake City, UT.

Missoula, MT: U.S. Department of Agriculture, Forest Service,

Equipment Development Center: 34–36.

Stevens, R.; Monsen, S. B.; James, G.; Jorgensen, K. R.; Davis, J. N.;

Oaks, W. R. 1985b. Naming and release of ‘Cedar’ Palmer penstemon for commercial production and marketing of seed. Washington, DC: U.S. Department of Agriculture, Soil Conservation

Service. 9 p.

Stevens, R.; Shaw, N.; Howard, C. G. 1985c. Important nonleguminous forbs for Intermountain range. In: Carlson, J. R.;

McArthur, E. D., eds. Proceedings: selected papers presented at

the 38th annual meeting, of the Society for Range Management,

range plant improvements in Western North America; 1985

February 14; Salt Lake City, UT. Denver, CO: Society for Range

Management: 210–220.

Tiedemann, A. R. 1985. Description and discussion of field tour

sites. In: Johnson, K. L., ed. Proceedings of the third Utah shrub

ecology workshop; 1983 August 30–31; Provo, UT. Logan: Utah

State University, College of Natural Resources: 59–61.

Tiedemann, A. R.; Clary, W. P. 1985. Nitrogen distribution in

north central Utah Gambel oak stands. In: Johnson, K. L., ed.

Proceedings of the third Utah shrub ecology workshop; 1983

August 30–31; Provo, UT. Logan: Utah State University, College of Natural Resources: 13–18.

Tiedemann, A. R.; Furniss, M. M. 1985. Soil and litter nutrient

responses to looper defoliation of curlleaf mountain mahogany.

Forest Science. 31: 382–388.

Wagstaff, F. J. 1985. Economics of using Gambel oak for firewood.

In: Johnson, K. L., ed. Proceedings of the third Utah shrub ecology

workshop; 1983 August 30–31; Provo, UT. Logan: Utah State

University, College of Natural Resources: 53–58.

Weber, D. J.; Davis, T. D.; McArthur, E. D.; Sankhla, N. 1985.

Chrysothamnus nauseosus (rubber rabbitbrush): multiple-use

shrub of the desert. Desert Plants. 7: 172–180, 208–210.

1986

Allen, P. S.; Davis, T. D. 1986. Determining seed quality of cicer

milkvetch (Astragalus cicer L.). Newsletter of the Association of

Official Seed Analysts. 60(1): 86–92.

Allen, P. S.; Meyer, S. 1986. Developing procedures for testing

wildland seed. Newsletter of the Association of Official Seed

Analysts. 60(3): 26–28.

Allen, P. S.; Meyer, S. C.; Wilson, G. R.; Davis, T. D.; Davis, J. N.;

Stevens, R.; Jorgensen, K. 1986a. Proposal: addition of Ceratoides

lanata—winterfat to the rules. Newsletter of the Association of

Official Seed Analysts. 60(1): 15–17.

Allen, P. S.; Meyer, S. C.; Wilson, G. R.; Davis, T. D.; Davis, J. N.;

Stevens, R.; Jorgensen, K. 1986b. Proposal: addition of Elymus

cinereus—basin wildrye to the rules. Newsletter of the Association of Official Seed Analysts. 60(1): 18–19.

Allen, P. S.; Meyer, S. C.; Wilson, G. R.; Davis, T. D.; Davis, J. N.;

Stevens, R.; Jorgensen, K. 1986c. Proposal: addition of Kochia

prostrata—forage kochia to the rules. Newsletter of the Association of Official Seed Analysts. 60(1): 19–20.

Allen, P. S.; Wilson, G. R.; Davis, T. D.; Davis, J. N.; Stevens, R.;

Jorgensen, K. 1986d. Proposal: addition of Astragalus cicer—

cicer milkvetch to the rules. Newsletter of the Association of

Official Seed Analysts. 60(1): 13–14.

Behan, B.; Welch, B. L. 1986. Winter nutritive content of black

sagebrush (Artemisia nova) grown in a uniform garden. Great

Basin Naturalist. 46: 161–165.

Buman, R. A. 1986. Seed germination and seedling interspecific

competition of mountain rye (Secale montanum Guss.), ‘Hycrest’

crested wheatgrass (Agropyron cristatum L. x A. desertorum

Fisch.) and downy brome (Bromus tectorum L.). Laramie: University of Wyoming. 48 p. Thesis.

Bunderson, E. D.; Weber, D. J.; Nelson, D. L. 1986a. Diseases

associated with Juniperus osteosperma and a model for predicting their occurrence with environmental site factors. Great Basin

Naturalist. 46: 427–440.

Bunderson, E. D.; Welch, B. L.; Weber, D. J. 1986b. In vitro

digestibility of Juniperus osteosperma (Torr.) Little from 17 Utah

sites. Forest Science. 32: 834–840.

Clary, W. P. 1986a. Black sagebrush response to grazing in the eastcentral Great Basin. In: McArthur, E. D.; Welch, B. L., comps.

Proceedings—symposium on the biology of Artemisia and

Chrysothamnus; 1984 July 9–13; Provo, UT. Gen. Tech. Rep.

INT-200. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Research Station: 181–185.

Clary, W. P. 1986b. Fifty-year response to grazing in the low-shrub

cold desert of the Great Basin, U.S.A. In: Joss, P. J.; Lynch, P. W.;

Williams, O. B., eds. Rangelands: a resource under siege: proceedings of the Second International Rangeland Congress; 1985 May

13–18; Adelaide, Australia. Canberra, Australia: Australian Academy of Science: 37–38.

Clary, W. P.; Tiedemann, A. R. 1986. Distribution of biomass within

small tree and shrub form Quercus gambelii stands. Forest

Science. 32: 234–242.

Davis, J. N.; Stevens, R. 1986. Comparison of production in twentyseven accessions of four sagebrush taxa. In: McArthur, E. D.;

Welch, B. L., comps. Proceedings—symposium on the biology of

Artemisia and Chrysothamnus; 1984 July 9–13; Provo, UT. Gen.

Tech. Rep. INT-200. Ogden, UT: U.S. Department of Agriculture,

Forest Service, Intermountain Research Station: 336–341.

Delany, D. 1986. Natural variation of Eriogonum niveum and its

relation to management of wildlife habitat. Seattle: University of

Washington. 160 p. Thesis.

Elderkin, R. L., Jr.; Dietz, D. R.; Welch, B. L.; Ralphs, P. M.;

Czarnecki, J. K. 1986. Irrigation by mine discharge water and

fertilization of big sagebrush: effects of nutritional composition,

production, and mule deer use. In: McArthur, E. D.; Welch, B. L.,

comps. Proceedings—symposium on the biology of Artemisia and

Chrysothamnus; 1984 July 9–13; Provo, UT. Gen. Tech. Rep.

INT-200. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Research Station: 140–145.

Frank, C. T.; Smith, B. N.; Welch, B. L. 1986. Photosynthesis,

growth, transpiration and 13C relationships among three

subspecies of big sagebrush. In: McArthur, E. D.; Welch, B.

L., comps. Proceedings—symposium on the biology of Artemisia and Chrysothamnus; 1984 July 9–13; Provo, UT. Gen.

Tech. Rep. INT-200. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station: 332–

335.

Goodrich, S. 1986a. Utah flora: Apiaceae (Umbelliferae). Great

Basin Naturalist. 46: 66–106.

Goodrich, S. 1986b. Vascular plants of the Desert Experimental

Range, Millard County, Utah. Gen. Tech. Rep. INT-209. Ogden,

UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station. 72 p.

Goodrich, S.; Neese, E. 1986. Uinta Basin flora. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Region. 319 p.

Hegerhorst, D. F. 1986. Chemical composition of Chrysothamnus

nauseosus. Provo, UT: Brigham Young University. 346 p. Thesis.

Hobbs, N. T.; Welch, B. L.; Remington, R. E. 1986. Effects of big

sagebrush on in vitro digestion of grass cell walls. In: McArthur,

E. D.; Welch, B. L., comps. Proceedings—symposium on the

biology of Artemisia and Chrysothamnus; 1984 July 9–13; Provo,

UT. Gen. Tech. Rep. INT-200. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Research Station:

186–189.

Larson, F. R.; Ffolliott, P. F.; Clary, W. P. 1986. Managing wildlife

habitat. Journal of Forestry. 84: 40–41.

McArthur, E. D. 1986. Specificity of galls on Chrysothamnus nauseosus subspecies. In: McArthur, E. D.; Welch, B. L., comps.

Proceedings—symposium on the biology of Artemisia and

Chrysothamnus; 1984 July 9–13; Provo, UT. Gen. Tech. Rep.

INT-200. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Research Station: 205–210.

McArthur, E. D.; Goodrich, S. K. 1986. Artemisia tridentata ssp.

spiciformis: distribution and taxonomic placement. In: McArthur,

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Forest Service, Intermountain Research Station: 55–57.

McArthur, E. D.; Monsen, S. B.; Blauer, A. C. 1986a. Inventory of and

rehabilitation recommendations for sites disturbed by modern man’s

activities in Grand Teton National Park. In: University of Wyoming

National Park Service Research Center Ninth Annual Report.

Laramie: University of Wyoming National Park Service Research

Center: 75–82.

McArthur E. D.; Sanderson, S. C.; Freeman, D. C. 1986b. Isozymes of an

autopolyploid shrub, Atriplex canescens (Chenopodiaceae). Great Basin

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Medin, D. E. 1986. Grazing and passerine breeding birds in a Great

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Meyer, S. E.; Allen, P. S.; Wilson, G. R.; Davis, T. D.; Davis, J. N.; Stevens,

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Monsen, S. B.; Shaw, N. 1986. Response of an alkali sagebrush/fescue

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Nelson, D. L.; Sturges, D. L. 1986. A snowmold disease of unknown

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Noller, G. L.; McArthur, E. D. 1986. Establishment and initial results

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Smith, C. B. 1986. Grazing effects and site factors in relation to grazing

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Stevens, R. 1986a. Are live pinyon and Utah juniper trees on chaining

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Stevens, R. 1986b. Population dynamics of two sagebrush

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Stranthan, S. E.; Monsen, S. B. 1986. Selection of a cultivar of

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Sturges, D. L.; Nelson, D. L. 1986. Snow depth and incidence of

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Wagstaff, F. J. 1986b. Economic issues of grazing and riparian

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Welch, B. L.; McArthur, E. D. 1986a. Growth rate of big

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Welch, B. L.; McArthur, E. D. 1986b. Wintering mule deer

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Welch, B. L.; McArthur, E. D.; Nelson, D. L.; Pederson, J. C.;

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Whisenant, S. G.; Clary, W. P. 1986. Spatial distribution of

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the Western Society of Weed Science. 39: 73–84.

Winkel, V. 1986. Habitat differences between mountain big sagebrush and mountain silver sagebrush in the Strawberry Valley

of central Utah. Provo, UT: Brigham Young University. 30 p.

Thesis.

Winward, A. H.; McArthur, E. D.; Kaffer, D. A.; Plummer, C. A.;

Brackley, G. K. 1986. Another sagebrush in Nevada. Tech. Notes

TN-Range NV-44. Reno, NV: U.S. Department of Agriculture,

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1987

Allen, P. S.; Meyer, S. E.; Davis, T. D. 1987. Determining seed

quality of winterfat (Ceratoides lanata [Pursh.] J. T. Howell).

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isotope 13C and plant vegetation patterns to moisture gradients

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Utah, U.S.A. Provo, UT: Brigham Young University. 41 p. Thesis.

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pinyon-juniper conference; 1986 January 13–16; Reno, NV. Gen.

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Clary, W. P.; Holmgren, R. C. 1987b. Reversal of desertification on

the low-shrub cold desert. In: Aldon, E. F.; Gonzales, V., Carlors,

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Davis, J. N. 1987. Seedling establishment biology and patterns of

interspecific association among established seeded and nonseeded species on a chained juniper-pinyon woodland in central

Utah. Provo, UT: Brigham Young University. 80 p. Dissertation.

Harper, K. T.; Sanderson, S. C.; McArthur, E. D. 1987. Vegetation

communities of Zion National Park. In: Eleventh annual report.

Laramie: University of Wyoming, National Park Service Research Center: 191–196.

Hegerhorst, D. F.; Weber, D. J.; McArthur, E. D. 1987a. Chemical

analysis and comparison of subspecies of Chrysothamnus

nauseosus and other related species. Biochemical Systematics

and Ecology. 15: 201–208.

Hegerhorst, D. F.; Weber, D. J.; McArthur, E. D. 1987b. Chemical

components of Chrysothamnus nauseosus: a preliminary report.

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Hegerhorst, D. F.; Weber, D. J.; McArthur, E. D. 1987c. Resin and

rubber content in Chrysothamnus. Southwestern Naturalist. 32:

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Jacobson, T. L. C.; Welch, B. L. 1987. Planting depth of ‘Hobble

Creek’ mountain big sagebrush seed. Great Basin Naturalist. 47:

497–499.

Kahn, M. A.; Sankhla, N.; Weber, D. J.; McArthur, E. D. 1987. Seed

germination characteristics of Chrysothamnus nauseosus ssp.

viridulus (Asterae, Asteraceae). Great Basin Naturalist. 47:

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Kitchen, S. G.; Meyer, S. E.; Wilson, G. R.; Davis, J. N.; Stevens, R.

1987. Addition of Hedysarum boreale—northern sweetvetch to

the rules. Newsletter of the Association of Official Seed Analysts.

61(1): 65–66.

McArthur, E. D.; Meyer, S. E. 1987. A review of the taxonomy and

distribution of Chrysothamnus. In: Johnson, K. L., ed. Proceedings of the fourth Utah shrub ecology workshop: the genus

Chrysothamnus; 1986 September 17–19; Cedar City, UT. Logan:

Utah State University, College of Natural Resources: 9–17.

McArthur, E. D.; Meyer, S. E.; Weber, D. J. 1987a. Germination rate

at low temperature: rubber rabbitbrush population differences.

Journal of Range Management. 40: 530–533.

McArthur, E. D.; Monsen, S. B.; Welch, B. L. 1987b. Shrubs and

forbs for revegetation plantings in the sagebrush ecosystem. In:

Onsager, J. A., ed. Integrated pest management in rangeland:

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March 27–28; Reno, NV. ARS-50. Washington, DC: U.S. Department of Agriculture, Agricultural Research Service: 28–39.

Meyer, S. E.; Kitchen, S. G.; Wilson, G. R.; Davis, J. N.; Stevens, R.

1987a. Addition of Amelanchier alnifolia—Saskatoon serviceberry to the rules. Newsletter of the Association of Official Seed

Analysts. 61(1): 66–68.

Meyer, S. E.; Kitchen, S. G.; Wilson, G. R.; Davis, J. N.; Stevens, R.

1987b. Addition of Elymus elmoides—bottlebrush squirreltail to

the rules. Newsletter of the Association of Official Seed Analysts.

61(1): 59–61.

Meyer, S. E.; Allen, P. A.; Wilson, G. R.; Davis, J. N.; Stevens, R.

1987c. Addition of Penstemon eatonii—firecracker penstemon to

the rules. Newsletter of the Association of Official Seed Analysts.

61(1): 61.

Meyer, S. E.; Allen, P. A.; Wilson, G. R.; Davis, J. N.; Stevens, R.

1987d. Addition of Penstemon palmeri—Palmer penstemon to the

rules. Newsletter of the Association of Official Seed Analysts.

61(1): 62.

Meyer, S. E.; Allen, P. A.; Wilson, G. R.; Davis, J. N.; Stevens, R.

1987e. Addition of Penstemon strictus—Rocky Mountain penstemon to the rules. Newsletter of the Association of Official Seed

Analysts. 61(1): 62–63.

Meyer, S. E.; Allen, P. A.; Wilson, G. R.; Davis, J. N.; Stevens, R.

1987f. Addition of Secale montanum—Mountain wildrye to the

rules. Newsletter of the Association of Official Seed Analysts.

61(1): 63–65.

Meyer, S. E.; McArthur, E. D. 1987. Studies on seed germination

biology of rubber rabbitbrush. In: Johnson, K. L., ed. Proceedings

of the fourth Utah shrub ecology workshop: the genus

Chrysothamnus. 1986 September 17–19; Cedar City, UT. Logan,

UT: Utah State University, College of Natural Resources: 19–25.

Meyer, S. E.; McArthur, E. D.; Monsen, S. B. 1987g. Infraspecific

variation in germination patterns of rangeland shrubs and its

relationship to seeding success. In: Frasier, G. W.; Evans, R., eds.

Seed and seedbed ecology of rangeland plants: proceedings of

symposium; 1987 April 21–23; Tucson, AZ. Tucson, AZ: U.S.

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Nelson, D. L. 1987. Susceptibility of antelope bitterbrush to seedbed

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seedbed ecology of rangeland plants: proceedings of symposium;

1987 April 21–23; Tucson, AZ. Tucson, AZ: U.S. Department of

Agriculture, Agricultural Research Service: 117–121.

O’Neal, G. T.; Flinders, J. T.; Clary, W. P. 1987. Behavioral ecology of

the Nevada kit fox (Vulpes macrotis nevadensis) on a managed

desert rangeland. In: Genoways, H. H., comp. Current Mammology,

volume 1. New York, NY: Pleunm Publishing Corporation: 443–481.

Pope, C. A., III; Wagstaff, F. J. 1987a. An economic evaluation of the

Oak Creek Range Management Area, Utah. Gen. Tech. Rep. INT224. Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Research Station. 14 p.

Pope, C. A., III; Wagstaff, F. J. 1987b. Economics of the Oak Creek

range management project. Journal of Environmental Management. 25: 157–165.

Provenza, F. D.; Flinders, J. T.; McArthur, E. D. 1987a. Introduction: plant-herbivore interactions. In: Provenza, F. D.; Flinders,

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U.S. Department of Agriculture, Forest Service, Intermountain

Research Station. 179 p.

Sanderson, S. C.; Pendleton, R. L.; McArthur, E. D.; Harper, K. T.

1987. Saponin effect on small mammal forage preference in a

planting of Atriplex canescens. In: Provenza, F. D.; Flinders, J. T.;

McArthur, E. D., comps. Proceedings—symposium on plantherbivore interactions; 1985 August 7–9; Snowbird, UT. Gen.

Tech. Rep. INT-222. Ogden, UT: U.S. Department of Agriculture,

Forest Service, Intermountain Research Station: 74–77.

Sankhla, N.; Davis, T. D.; Weber, D. J.; McArthur, E. D. 1987.

Biology and economic botany of Chrysothamnus (rabbitbrush): a

potentially useful shrub for arid regions. Journal of Economic and

Taxonomic Botany. 10: 481–496.

Stevens, R. 1987. Thirty years of pinyon-juniper big game habitat

improvement projects: what have we learned? In: Everett, R. L.,

comp. Proceedings—pinyon-juniper conference; 1986 January

13–16; Reno, NV. Gen. Tech. Rep. INT-215. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Research Station: 558–571.

Stutz, H. C.; Sanderson, S. C.; McArthur, E. D.; Ge-lin, C. 1987.

Chromosome races of Grayia brandegei (Chenopodiaceae).

Madroño. 34: 142–149.

Thorderson, L. G. 1987. Restoring estimability in designs with

missing cells: an application to the analysis of livestock grazing

patterns in southwestern Utah. Provo, UT: Brigham Young

University. 79 p. Thesis.

Tiedemann, A. R.; Clary, W. P.; Barbour, R. J. 1987a. Underground

systems of Gambel oak (Quercus gambelii) in central Utah.

American Journal of Botany. 74: 1065–1071.

Tiedemann, A. R.; McArthur, E. D.; Freeman, D. C. 1987b. Variations in physiological metabolites and chlorophyll in sexual

phenotypes of ‘Rincon’ fourwing saltbush. Journal of Range

Management. 40: 151–155.

Wagstaff, F. J. 1987. Economics of managing pinyon-juniper lands

for woodland products. In: Everett, R. L., comp. Proceedings—

pinyon-juniper conference; 1986 January 13–16; Reno, NV. Gen.

Tech. Rep. INT-215. Ogden, UT: U.S. Department of Agriculture,

Forest Service, Intermountain Research Station: 168–172.

Wagstaff, F. J.; Pope, C. A., III. 1987. Finding the appropriate forage

value for analyzing the feasibility of public range improvements.

Res. Pap. INT-378. Ogden, UT: U.S. Department of Agriculture,

Forest Service, Intermountain Research Station. 4 p.

Weber, D. J.; Hegerhorst, D. F.; Davis, T. D.; McArthur, E. D. 1987.

Potential uses of rubber rabbitbrush (Chrysothamnus nauseosus).

In: Johnson, K. L., ed. Proceedings of the fourth Utah shrub

ecology workshop: the genus Chrysothamnus. 1986 September

17–19; Cedar City, UT. Logan: Utah State University, College of

Natural Resources: 27–33.

Welch, B. L.; McArthur, E. D.; Rodriquez, R. L. 1987. Variation in

utilization of big sagebrush accessions by wintering sheep. Journal of Range Management. 40: 113–115.

Welsh, S. L.; Atwood, N. D.; Goodrich, S.; Higgins, L. C., eds. 1987.

A Utah flora. Great Basin Naturalist Memoir No. 9. Provo, UT:

Brigham Young University. 894 p.

Whisenant, S. G.; Clary, W. P. 1987. Tebuthiuron distribution in

soil following application of pellets. Journal of Environmental

Quality. 16: 397–402.

1988

Buman, R. A.; Monsen, S. B.; Abernathey, R. H. 1988. Seedling

competition between mountain rye, Hycrest crested wheatgrass,

and downy brome. Journal of Range Management. 41: 30–34.

Clary, W. P.; Welch, B. L.; Booth, G. D. 1988. In vitro digestion

experiments: importance of variation between inocula donors.

Journal of Wildlife Management. 52: 358–361.

Haws, B. A.; Roe, A. H.; Nelson, D. L. 1988. Index to information on

insects associated with western wildland shrubs. Gen. Tech. Rep.

INT-248. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Research Station. 296 p.

Hegerhorst, D. F.; Bhat, R. B.; Weber, D. J.; McArthur, E. D. 1988a.

Seasonal changes of selected secondary plant products in

Chrysothamnus nauseosus ssp. turbinatus. Great Basin Naturalist. 48: 1–8.

Hegerhorst, D. F.; Weber, D. J.; Bhat, R. B.; Davis, T. D.; Sanderson,

S. C.; McArthur, E. D. 1988b. Seasonal changes in rubber and

resin contents in Chrysothamnus nauseosus ssp. hololeucus and

ssp. turbinatus. Biomass. 15: 133–142.

Huang, J.; Hess, W. M.; Weber, D. J.; McArthur, E. D.; Meyer, S. E.;

Seegmiller, R. 1988. Computer analysis of cross sections of leaves

of Chrysothamnus taxa and their relation to environmental

conditions. Great Basin Naturalist. 48: 334–347.

Kitchen, S. G. 1988. Germination studies with fifteen species of

Intermountain penstemons. Provo, UT: Brigham Young University. 82 p. Thesis.

McArthur, E. D. 1988. New plant development in range management. In: Tueller, P. T., ed. Vegetation science applications for

rangeland analysis and management. Handbook of Vegetation

Science 14. Dordrecht, Netherlands: Kluwer Academic Publishers: 81–112.

McArthur, E. D.; Blauer, A. C.; Sanderson, S. C. 1988a. Mule deerinduced mortality of mountain big sagebrush. Journal of Range

Management. 41: 114–117.

McArthur, E. D.; Welch, B. L.; Sanderson, S. C. 1988b. Natural and

artificial hybridization between big sagebrush (Artemisia tridentata) subspecies. Journal of Heredity. 79: 268–276.

Meyer, S. E.; Kitchen, S. G.; Wilson, G. R.; Stevens, R. 1988a.

Proposal: addition of Artemisia ludoviciana—Louisiana sagewort

to the rules. Newsletter of the Association of Official Seed Analysts. 62(1): 15–16.

Meyer, S. E.; Kitchen, S. G.; Wilson, G. R.; Stevens, R. 1988b.

Proposal: addition of Artemisia nova—(syn. Artemisia arbuscula

subsp. nova) black sagebrush to the rules. Newsletter of the

Association of Official Seed Analysts. 62(1): 16–17.

Meyer, S. E.; Kitchen, S. G.; Wilson, G. R.; Stevens, R. 1988c.

Proposal: addition of Artemisia tridentata—big sagebrush to the

rules. Newsletter of the Association of Official Seed Analysts.

62(1): 17–18.

Meyer, S. E.; Kitchen, S. G.; Wilson, G. R.; Stevens, R. 1988d.

Proposal: addition of Ephreda viridis—green Mormon tea to the

rules. Newsletter of the Association of Official Seed Analysts.

62(1): 17–18.

Pendleton, R. L.; McArthur, E. D.; Freeman, D. C.; Blauer, A. C. 1988.

Heterodichogamy in Grayia brandegiei (Chenopodiaceae): report

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Department of Agriculture, Forest Service, Intermountain Research Station: 167–170.

Welch, B. L.; Wagstaff, F. J.; Williams, R. L. 1990b. Sage grouse

status and recovery plan for Strawberry Valley, Utah. Res. Pap.

INT-430. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Research Station. 10 p.

1991

Carlson, J. R.; Cunningham, R. A.; Everett, H. W.; Jacobsen, E. T.;

Lorenz, D. G.; McArthur, E. D. 1991. Conservation tree and shrub

cultivars in the United States. Agric. Handb. 692. Washington,

DC: U.S. Department of Agriculture, Soil Conservation Service.

50 p.

Chu, G-L.; Stutz, H. C.; Sanderson, S. C. 1991. Morphology and

taxonomic position of Suckeya suckleyana (Chenopodiaceae).

American Journal of Botany. 78: 63–68.

Davis, J. N.; Brotherson, J. D. 1991. Ecological relationships of

curlleaf mountain-mahogany (Cercocarpus ledifolius Nutt.) communities in Utah and implications for management. Great Basin

Naturalist. 51: 153–166.

Freeman, D. C.; Turner, W. A.; McArthur, E. D.; Graham, J. H. 1991.

Characterization of a narrow hybrid zone between two subspecies

of big sagebrush (Artemisia tridentata: Asteraceae). American

Journal of Botany. 78: 805–815.

Kitchen, S. G.; Meyer, S. E. 1991. Seed germination of Intermountain penstemons as influenced by stratification and GA3 treatments. Journal of Environmental Horticulture. 9: 51–56.

McArthur, E. D. 1991. Intermountain consortium for arid lands

research formed. Great Basin Naturalist. 51: 300.
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Megahan, W. F.; Monsen, S. B.; Wilson, M. D. 1991. Probability of

sediment yields form surface erosion on granitic roadfills in

Idaho. Journal of Environmental Quality. 20: 53–60.

Meyer, S. E.; Monsen, S. B. 1991. Habitat-correlated variation in

mountain big sagebrush (Artemisia tridentata ssp. vaseyana)

seed germination patterns. Ecology. 72: 739–742.

Tippets, D.; Anderson, V. J. 1991. Partnership preserves historic

range research sites. Rangelands. 13: 121–124.

Wagstaff, F. J.; Welch, B. L. 1991. Seedstalk production of mountain

big sagebrush enhanced through short-term protection from

heavy browsing. Journal of Range Management. 44: 72–74.

Welch, B. L.; Wagstaff, F. J.; Roberson, J. A. 1991. Preference of

wintering sage grouse for big sagebrush. Journal of Range Management. 44: 462–465.

Whisenant, S. G.; Wagstaff, F. J. 1991. Successional trajectories of

a grazed salt desert shrubland. Vegetatio. 94: 133–140.

1992

Byrd, D. W. 1992. Biochemical assessment of the hybrid zone formed

by Artemisia tridentata tridentata and Artemisia tridentata

vaseyana using an automated gas chromatography-data system

and statistical methods. Detroit, MI: Wayne State University. 57 p.

Thesis.

Clary, W. P.; McArthur, E. D. 1992. Introduction: ecology and

management of riparian shrub communities. In: Clary, W. P.;

McArthur, E. D.; Bedunah, D; Wambolt, C. L., comps. Proceedings—symposium on ecology and management of riparian shrub

communities; 1991 May 29–31; Sun Valley, ID. Gen. Tech. Rep.

INT-289. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Research Station: 1–2.

Clary, W. P.; McArthur, E. D.; Bedunah, D.; Wambolt, C. L., comps.

1992. Proceedings—symposium on ecology and management of

riparian shrub communities; 1991 May 29–31; Sun Valley, ID.

Gen. Tech. Rep. INT-289. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station. 232 p.

Gunasekaran, M.; Weber, D. J.; Sanderson, S. C.; Devall, M. M.

1992. Reanalysis of the vegetation of Been Branch Gorge Research Natural Area, a hemlock-beech community on the Warrior

River Basin of Alabama. Castanea. 57: 34–45.

Harper, K. T.; Sanderson, S. C.; McArthur, E. D. 1992. Riparian

ecology in Zion National Park, Utah. In: Clary, W. P.; McArthur,

E. D.; Bedunah, D; Wambolt, C. L., comps. Proceedings—symposium on ecology and management of riparian shrub communities;

1991 May 29–31; Sun Valley, ID. Gen. Tech. Rep. INT-289.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Research Station: 32–41.

Kitchen, S. G.; Meyer, S. E. 1992. Temperature-mediated changes

in seed dormancy and light requirement for Penstemenonpalmeri

(Scrophulariaceae). Great Basin Naturalist. 52: 53–58.

McArthur, E. D. 1992. In memoriam—A. Perry Plummer (1911–

1991): teacher, naturalist, range scientist. Great Basin Naturalist. 52: 1–10.

McArthur, E. D.; Freeman, D. C.; Luckinbill, L. S.; Sanderson, S. C.;

Noller, G. L. 1992. Are trioecy and sexual liability in Atriplex

canescens genetically based: evidence from clonal studies. Evolution. 46: 1708–1721.

McArthur, E. D.; Sanderson, S. C. 1992a. A comparison between

xeroriparian and upland vegetation of Beaver Dam Slope,

Utah. In: Clary, W. P.; McArthur, E. D.; Bedunah, D; Wambolt,

C. L., comps. Proceedings—symposium on ecology and management of riparian shrub communities; 1991 May 29–31; Sun

Valley, ID. Gen. Tech. Rep. INT-289. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research

Station: 25–31.

McArthur, E. D.; Sanderson, S. C. 1992b. Great Sand Dune National

Monument vegetation patterns. In: 15th annual report, 1991.

Laramie: University of Wyoming, National Park Service Research Center: 185–189.

Medin, D. E. 1992. Birds of a Great Basin sagebrush habitat in eastcentral Nevada. Res. Pap. INT-452. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Research Station. 4 p.

Megahan, W. F.; Monsen, S. B.; Wilson, M. C.; Lozano, N.; Haber, D.

F.; Booth, G. D. 1992. Erosion control practices applied to granitic

roadfills for forest roads in Idaho: cost effectiveness evaluation.

Land Degradation and Rehabilitation. 3: 55–65.

Meyer, S. E. 1992. Habitat correlated variation in firecracker penstemon (Penstemon eatonii Gray: Scophulariaceae) seed germination

response. Bulletin of the Torrey Botanical Club. 119: 268–279.

Meyer, S. E.; Kitchen, S. G. 1992. Cyclic seed dormancy in the shortlived perennial Penstemon palmeri. Journal of Ecology. 80: 115–122.

Meyer, S. E.; Monsen, S. B. 1992. Big sagebrush germination

patterns: subspecies and population differences. Journal of Range

Management. 45: 87–93.

Mikhiel, G. S.; Meyer, S. E.; Pendleton, R. L. 1992. Variation in

germination response to temperature and salinity in shrubby

Atriplex species. Journal of Arid Environments. 22: 39–49.

Monsen, S. B.; Meyer, S. E.; Carlson, S. C. 1992. Sagebrush

establishment enhanced by snowfencing. In: U.S. Department

of Agriculture, Forest Service, 1992 annual report, Rangeland

Technology Equipment Council; 1992 February 9; Spokane,

WA. Missoula, MT: U.S. Department of Agriculture, Forest

Service, Missoula Technology and Equipment Development

Center: 6–8.

Nasr, M. A.; Monsen, S. B.; Meyer, S. E.; Belal, A. H. 1992. Effects

of salt and temperature on germination of cheatgrass and small

burnet. Egyptian Journal of Applied Science. 7(2): 1–10.

Pendleton, B. K.; Freeman, D. C.; McArthur, E. D.; Pendleton, R. L.

1992a. Life history features of three sexual morphs of Atriplex

canescens (Chenopodiaceae) clones grown in a common garden.

American Journal of Botany. 79: 376–382.

Pendleton, R. L.; Frischknecht, N. C.; McArthur, E. D. 1992b. Longterm survival of 20 selected plant accessions in a Rush Valley, Utah,

planting. Res. Note INT-403. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Research Station. 7 p.

Pendleton, R. L.; Wagstaff, F. J.; Welch, B. L. 1992c. Winter nutrient

content and deer use of Gambel oak twigs in north central Utah.

Great Basin Naturalist. 52: 293–299.

Stevens, A. R. 1992. Establishment and distribution of forage

kochia seedlings within crested wheatgrass stands. Provo, UT:

Brigham Young University. 38 p. Thesis.

Stevens, R.; McArthur, E. D.; Davis, J. N. 1992. Reevaluation of

vegetative cover changes, erosion, and sedimentation on two

watersheds—1912–1983. In: Clary, W. P.; McArthur, E. D.;

Bedunah, D; Wambolt, C. L., comps. Proceedings—symposium on

ecology and management of riparian shrub communities; 1991

May 29–31; Sun Valley, ID. Gen. Tech. Rep. INT-289. Ogden, UT:

U.S. Department of Agriculture, Forest Service, Intermountain

Research Station: 123–128.

Weber, D. J.; Nelson, D. L. 1992. Die-off of Utah juniper: Natural

Bridges National Monument. In: 15th annual report, 1991.

Laramie: University of Wyoming, National Park Service Research Center: 205–208.

Welch, B. L.; Nelson, E. D.; Young, S. A.; Sands, A. R.; Wagstaff, F.

J.; Nelson, D. L. 1992a. ‘Gordon Creek’—a superior, tested

germplasm of Wyoming big sagebrush. Res. Pap. INT-461. Ogden,

UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station. 7 p.

Welch, B. L.; Wagstaff, F. J. 1992. ‘Hobble Creek’ big sagebrush vs.

antelope bitterbrush as a winter forage. Journal of Range Management. 45: 140–142.

Welch, B. L.; Young, S. A.; Shields, P. W. 1992b. ‘Hobble Creek’

mountain big sagebrush. In: Habitat Express 92-1. Ogden, UT:

U.S. Department of Agriculture, Forest Service, Intermountain

Region. 6 p.

Yorks, T. P.; West, N. E.; Capels, K. M. 1992. Vegetation differences

in desert shrublands of western Utah’s Pine Valley between

1933–1989. Journal of Range Management. 45: 569–578.

1993

Allen, P. S.; Debaene, S. B. G.; Meyer, S. E. 1993. Regulation of grass

seed germination under fluctuating moisture regimes. In: Dome,

D.; Corbineau, F., eds. Fourth international workshop on seeds,

basic and applied aspects of seed biology; 1992 July 20–14; Anger,

France. Paris, France: Universite Pierre et Marie Curie: 387–392.

Anderson, V. J.; Thompson, R. M. 1993. Chemical and mechanical

control of false hellebore (Veratrum californicum) in an alpine
32 USDA Forest Service Proceedings RMRS-P-21. 2001

McArthur The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective

community. Res. Pap. INT-469. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Research Station. 6 p.

Baskin, C. C.; Baskin, J. M.; Meyer, S. E. 1993. Seed dormancy in the

Colorado Plateau shrub Mahonia freemontii (Berberidaceae) and

its ecological and evolutionary implications. Southwestern Naturalist. 38: 91–99.

Belal, A. H.; Rammah, A. M.; Hopkin, M. S.; Hansen, L. D.;

McArthur, E. D. 1993. Studies of salt-tolerance and chemical

analysis of fodder shrubs in Egypt and Utah (USA). In: Lieth, H.;

Al Massoom, A., eds. Towards a rational use of high salinity

tolerant plants, volume 2. Dordrecht, Netherlands: Kluwer Academic Publishers: 213–220.

Belnap, J. 1993. Recovery rates of cryptobiotic crusts: inoculant use

and assessment methods. Great Basin Naturalist. 53: 89–95.

Belnap, J.; Gardner, J. S. 1993. Soil microstructure in soils of the

Colorado Plateau: the role of cyanobacterium Microcoleus

vaginatus. Great Basin Naturalist. 53: 40–47.

Blauer, A. C.; McArthur, E. D.; Stevens, R.; Nelson, S. D. 1993.

Evaluation of roadside stabilization and beautification plantings

in south-central Utah. Res. Pap. INT-462. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Research Station. 65 p.

Chambers, J. C.; Norton, B. E. 1993. Effects of grazing and drought

on population dynamics of salt desert shrub species on the Desert

Experimental Range, Utah. Journal of Arid Environments. 24:

261–275.

Freeman, D. C.; McArthur, E. D.; Sanderson, S. C.; Tiedemann, A. R.

1993a. Influence of topography on cumulative pollen flow of

fourwing saltbush. Res. Note INT-413. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research

Station. 9 p.

Freeman, D. C.; McArthur, E. D.; Sanderson, S. C.; Tiedemann, A. R.

1993b. The influence of topography on male and female fitness

components of Atriplex canescens. Oecologia. 93: 538–547.

Harper, K. T.; Pendleton, R. L. 1993. Cyanobacteria and cyanolichens:

can they enhance availability of essential minerals for higher

plants. Great Basin Naturalist. 53: 59–72.

Haws, B. A.; Bohart, G. E.; Nelson, C. R.; Nelson, D. L. 1993. Insects

and their relationship to widespread shrub-dieoff in the Intermountain West of North America. In: Gaston, A.; Kenick, M.; Le

Honérou, eds. Proceedings of the Fourth International Rangeland Congress; 1991 April 22–26; Montpellier, France. Montpellier,

France: Association Francaise de Pastoralisme: 474–478.

McArthur, E. D. 1993. Shrub genetic diversity and development. In:

Gaston, A.; Kenick, M.; Le Honérou, eds. Proceedings of the

Fourth International Rangeland Congress; 1991 April 22–26;

Montpellier, France. Montpellier, France: Association Francaise

de Pastoralisme: 392–396.

Meyer, S. E.; Monsen, S. B. 1993. Genetic considerations in propagating native shrubs, forbs, and grasses from seed. In: Landis, T. D.,

tech. coord. Proceedings, Western Forest Nursery Association;

1992 September 14–18; Fallen Leaf, CA. Gen. Tech. Rep. RM-221.

Fort Collins, CO: U.S. Department of Agriculture, Forest Service,

Rocky Mountain Forest and Range Experiment Station: 47–54.

Monsen, S. B.; Anderson, V. J. 1993. A 52-year ecological history of

selected introduced and native grasses planted in central Idaho.

In: Proceedings of the XVII International Grassland Congress;

1993 February 8–21; Palmerston North, New Zealand. Palmerston

North, New Zealand: Keeling & Mundy (1983) Ltd.: 1740–1741.

Pellant, M.; Monsen, S. B. 1993. Rehabilitation on public rangelands in Idaho, USA: a change in emphasis from grass monocultures. In: Proceedings of the XVII International Grassland

Congress; 1993 February 8–21, Palmerston North, New Zealand.

Palmerston North, New Zealand: Keeling & Mundy (1983) Ltd.:

778–779.

Stutz, H. C. Chu, G-L.; Sanderson, S. C. 1993. Resurrection of the

genus Endolepis and clarification of Atriplex phyllostegia

(Chenopodiaceae). American Journal of Botany. 80: 592–597.

Walker, S. C. 1993. Effects of cattle and big game on the secondary

succession of aspen-conifer understory following fire. Provo, UT:

Brigham Young University. 44 p. Thesis.

Weber, D. J.; Hegerhorst, D. F.; Bhat, R. B.; McArthur, E. D. 1993.

Rubber rabbitbrush (Chrysothamnus nauseosus), a multi-use

desert shrub. In: Lieth, H.; Al Massoom, A., eds. Towards a

rational use of high salinity tolerant plants, volume 2. Dordrecht,

Netherlands: Kluwer Academic Publishers: 343–350.

Weber, D. J.; Nelson, D. L. 1993. Die-off of Utah Juniper: Natural

Bridges National Monument. In: Sixteenth annual report, 1992.

Laramie: University of Wyoming, National Park Service Research Center: 167–171.

Welch, B. L. 1993. Strategies for maintenance and restoration of

soil, water, flora, and fauna resources in a cold temperate rangeland. I. Grass is not always king; manage for diversity. In:

Proceedings of the XVII International Grassland Congress; 1993

February 8–21; Palmerston North, New Zealand. Palmerston

North, New Zealand: Keeling & Mundy (1983) Ltd.: 1775–1777.

1994

Allen, P. S., Debaene-Gill, S. B.; Meyer, S. E. 1994. Regulation of

germination timing in faculatively fall-emerging grasses. In:

Monsen, S. B.; Kitchen, S. G., comps. Proceedings—ecology and

management of annual rangelands; 1992 May 18–21; Boise, ID.

Gen. Tech. Rep. INT-GTR-313. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Research Station:

215–219.

Austin, D. D.; Stevens, R.; Jorgensen, K. R.; Urness, P. J. 1994.

Preferences of mule deer for 16 grasses found on Intermountain

winter ranges. Journal of Range Management. 47: 308–311.

Beckstead, J. 1994. Between-population differences in the germination ecophysiology of cheatgrass (Bromus tectorum) and

squirreltail (Elymus elmoides) during after-ripening. Provo, UT:

Brigham Young University. 101 p. Thesis.

Belnap, J.; Harper, K. T.; Warren, S. D. 1994. Surface disturbance

cyrptobiotic soil crusts: nitrogenase activity, chlorophyll content,

and chlorophyll degradation. Arid Soil Research and Rehabilitation. 8: 1–8.

Criddle, R. S.; Hopkin, M. S.; McArthur, E. D.; Hansen, L. D. 1994.

Plant distribution and the temperature coefficient of metabolism.

Plant, Cell, and Environment. 17: 233–243.

Davis, J. N. 1994a. Curlleaf mountain-mahogany: SRM 415. In:

Shiflet, T. N., ed. Rangeland cover types of the United States.

Denver, CO: Society for Range Management: 54–55.

Davis, J. N. 1994b. Littleleaf mountain-mahogany: SRM 417. In:

Shiflet, T. N., ed. Rangeland cover types of the United States.

Denver, CO: Society for Range Management: 56.

Davis, J. N. 1994c. Mountain-mahogany types. In: Shiflet, T. N., ed.

Rangeland cover types of the United States. Denver, CO: Society

for Range Management: 54.

Davis, J. N. 1994d. True mountain-mahogany: SRM 416. In: Shiflet,

T. N., ed. Rangeland cover types of the United States. Denver, CO:

Society for Range Management: 55–56.

Hall, D. B. 1994. Shrub recruitment inhibition in different herbaceous understories. Provo, UT: Brigham Young University. 58 p.

Thesis.

Harper, K. T.; McArthur, E. D. 1994. Gambel oak: SRM 413. In:

Shiflet, T. N., ed. Rangeland cover types of the United States.

Denver, CO: Society for Range Management: 51–53.

Katzner, T. E. 1994. Winter ecology of the pygmy rabbit (Brachylagus

idahoensis) in Wyoming. Laramie: University of Wyoming. 125 p.

Thesis.

Kitchen, S. G. Perennial forb life-history strategies on semiarid

rangelands: implications for revegetation. In: Monsen, S. B.;

Kitchen, S. G., comps. Proceedings—ecology and management of

annual rangelands; 1992 May 18–21; Boise, ID. Gen. Tech. Rep.

INT-GTR-313. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station: 342–346.

Kitchen, S. G.; Monsen, S. B. 1994. Germination rate and emergence

success in bluebunch wheatgrass. Journal of Range Management. 47: 145–150.

Klemmedson, J. O.; Tiedemann, A. R. 1994. Soil and vegetation

development in an abandoned sheep corral on degraded subalpine rangeland. Great Basin Naturalist. 54: 301–312.

McArthur, E. D. 1994. Ecology, distribution, and values of sagebrush within the Intermountain region. In: Monsen, S. B.; Kitchen,

S. G., comps. Proceedings—ecology and management of annual

rangelands; 1992 May 18–21; Boise, ID. Gen. Tech. Rep. INTGTR-313. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Research Station: 347–351.

McArthur, E. D.; Sanderson, S. C.; Webb, B. L. 1994. Nutritive quality

and mineral content of potential desert tortoise food plants. Res.
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Pap. INT-473. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Research Station. 26 p.

Meyer, S. E. 1994. Germination and establishment ecology of big

sagebrush; implications for community restoration. In: Monsen,

S. B.; Kitchen, S. G., comps. Proceedings—ecology and management of annual rangelands; 1992 May 18–21; Boise, ID. Gen.

Tech. Rep. INT-GTR-313. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station: 244–251.

Meyer, S. E.; Kitchen, S. G. 1994a. Life history variation in blue flax

(Linum perenne: Linaceae): seed germination phenology. American Journal of Botany. 81: 528–535.

Meyer, S. E.; Kitchen, S. G. 1994b. Habitat-correlated variation in

seed germination response to chilling in Penstemon section Glabri

(Scrophulariaceae). American Midland Naturalist. 132: 349–365.

Monsen, S. B. 1994a. Selection of plants for fire suppression on

semiarid sites. In: Monsen, S. B.; Kitchen, S. G., comps. Proceedings—ecology and management of annual rangelands; 1992 May

18–21; Boise, ID. Gen. Tech. Rep. INT-GTR-313. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Research Station: 363–373.

Monsen, S. B. 1994b. The competitive influences of cheatgrass

(Bromus tectorum) on site restoration. In: Monsen, S. B.; Kitchen,

S. G., comps. Proceedings—ecology and management of annual

rangelands; 1992 May 18–21; Boise, ID. Gen. Tech. Rep. INTGTR-313. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Research Station: 43–50.

Monsen, S. B.; Kitchen, S. G., comps. 1994. Proceedings—ecology and

management of annual rangelands; 1992 May 18–21; Boise, ID.

Gen. Tech. Rep. INT-GTR-313. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Research Station. 416 p.

Mudge, J. 1995. A genetic map of Saccharum officinarum(La Purple)

using RAPD single-dose markers. Provo, UT: 33 p. Thesis.

Pendleton, B. K.; Freeman, D. C.; McArthur, E. D.; Pendleton, R. L.

1994. Growth, reproduction, and life history features of fourwing

saltbush grown in a common garden. In: Monsen, S. B.; Kitchen,

S. G., comps. Proceedings—ecology and management of annual

rangelands; 1992 May 18–21; Boise, ID. Gen. Tech. Rep. INTGTR-313. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Research Station: 136–139.

Pendleton, R. L.; McArthur, E. D. 1994. Reproductive biology of

bitterbrush: interaccessional hybridization grown in a common

garden. In: Monsen, S. B.; Kitchen, S. G., comps. Proceedings—

ecology and management of annual rangelands; 1992 May 18–21;

Boise, ID. Gen. Tech. Rep. INT-GTR-313. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research

Station: 268–270.

Sanderson, S. C.; Stutz, H. C. 1994a. High chromosome numbers

in Mojavean and Sonoran Desert Atriplex canescens

(Chenopodiaceae). American Journal of Botany. 81: 1045–1053.

Sanderson, S. C.; Stutz, H. D. 1994b. Woody chenopods useful for

rangeland reclamation in Western North America. In: Monsen,

S. B.; Kitchen, S. G., comps. Proceedings—ecology and management of annual rangelands; 1992 May 18–21; Boise, ID. Gen. Tech.

Rep. INT-GTR-313. Ogden, UT: U.S. Department of Agriculture,

Forest Service, Intermountain Research Station: 374–378.

Stevens, R. 1994. Interseeding and transplanting to enhance

species composition. In: Monsen, S. B.; Kitchen, S. G., comps.

Proceedings—ecology and management of annual rangelands;

1992 May 18–21; Boise, ID. Gen. Tech. Rep. INT-GTR-313.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Research Station: 300–306.

Stevens, R.; Jorgensen, K. R. 1994. Rangeland species germination

through 25 and up to 40 years. In: Monsen, S. B.; Kitchen, S. G.,

comps. Proceedings—ecology and management of annual rangelands; 1992 May 18–21; Boise, ID. Gen. Tech. Rep. INT-GTR-313.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Research Station: 257–265.

Stutz, H. C.; Chu, G-L.; Sanderson, S. C. 1994. Atriplex asterocarpa

(Chenopodiace), a new species from southern Utah and northern

Arizona. Madroño. 41: 199–204.

Upper Colorado Environmental Plant Center; Utah Division of

Wildlife Resources: Colorado Agricultural Experiment Station—

Colorado State University; Utah Agricultural Experiment Station—Utah State University; U.S. Department of Agriculture,

Forest Service, Intermountain Research Station—Shrub Sciences Laboratory; U.S. Department of Agriculture, Agricultural

Research Service—Forage and Range Research Laboratory; U.S.

Department of Agriculture—Soil Conservation Service—Ecological Sciences Division. 1994. Notice of naming and release of

‘Timp’ Utah sweetvetch (Hedysarum boreale Nutt.) for soil improvement and early spring forage for both wildlife and livestock.

Meeker, CO: Upper Colorado Environmental Plant Center. 4 p.

Weber, D. J.; Gang, D. R.; Halls, S. C.; Smith, B. N.; McArthur, E. D.

1994. Inheritance of hydrocarbons in subspecific big sagebrush

(Artemisia tridentata) hybrids. Biochemical Systematics and

Ecology. 22: 689–697.

Welch, B. L. 1994. Rangeland shrubs. In: Arntzen, C. J., ed. Encyclopedia of agricultural science, volume 3. San Diego, CA: Academic Press: 575–586.

Welch, B. L.; Briggs, S. F.; Young, S. A. 1994. Pine Valley Ridge

source—a superior selected germplasm of black sagebrush. Res.

Pap. INT-474. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station. 9 p.

Welsh, S. L. 1994. New taxa and new nomenclatural combinations

in the Utah flora. Rhodora. 95: 392–421.

Yorks, T. P.; West, N. E.; Capels, K. M. 1994. Changes in pinyonjuniper woodlands in western Utah’s Pine Valley between 1933–

1989. Journal of Range Management. 47: 359–364.

1995

Allen, P. S.; Meyer, S. E.; Beckstead, J. 1995. Patterns of seed afterripening in Bromus tectorum. Journal of Experimental Botany.

46: 1737–1744.

Beckstead, J.; Meyer, S. E.; Allen, P. S. 1995. Effects of afterripening on cheatgrass (Bromus tectorum) and squirreltail (Elymus

elmoides) germination. In: Roundy, B. A.; McArthur, E. D.; Haley,

J. S.; Mann, D. K., comps. Proceedings: wildland shrub and arid

land restoration symposium; 1993 October 19–21; Las Vegas, NV.

Gen. Tech. Rep. INT-GTR-315. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Research Station:

165–172.

Belnap, J.; Harper, K. T. 1995. Influence of cryptobiotic soil crusts

on elemental content of tissue of two desert seed plants. Arid Soil

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Freeman, D. C.; Emlen, J. M. 1995. Assessment of interspecific

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Grover, M. C.; DeFalco, L. A. 1995. Desert tortoise (Gopherus

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national meeting of the American Society for Surface Mining and

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Moore, K. D. 1995. Effects of seed size on germination and emergence of burnet (Sanguisorba) Scop. (Rosaceae) and variation in

drought tolerance within and among ecotypes of small burnet

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University. 76 p. Thesis.

Pendleton, B. K.; Meyer, S. E.; Pendleton, R. L. 1995. Blackbrush

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Ramsey, T.; Stutz, H. C.; Nelson, D. L. 1995. Seeding failure in

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Shaw, N. L.; Monsen, S. B. 1995. ‘Lassen’ antelope bitterbrush. In:

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Service, Intermountain Research Station: 364–371.

Thacker, R. K. 1995. Comparison and use of four techniques for

censusing three sub-species of kit fox. Provo, UT: Brigham Young

University. 71 p. Thesis.

Walker, S. C.; Stevens, R.; Monsen, S. B.; Jorgensen, K. R. 1995.

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Weber, D. J.; Gang, D.; Halls, S.; Nelson, D. L. 1995. Juniper decline

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Welch, B. L. 1995. Beyond twelve percent purity. In: Roundy, B. A.;

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UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station: 126–129.

Welch, B. L.; Cox, C. L.; Sales, T. K. 1995. Strutting sounds and

strutting posturing of two Utah sage grouse populations. Res.

Pap. INT-RP-485. Ogden, UT: U.S. Department of Agriculture,

Forest Service, Intermountain Research Station. 8 p.

Welch, B. L.; Nelson, D. L. 1995. Black stem rust reduces big

sagebrush seed production. Journal of Range Management. 48:

398–401.

Winward, A. H.; McArthur, E. D. 1995. Lahontan sagebrush (Artemisia arbuscula ssp. longicaulis): a new taxon. Great Basin

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Young, S. A.; Kitchen, S. G.; Armstrong, G.; Watson, V. 1995.

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1996

Alzerreca-Angelo, H. 1996. Spatial and temporal dynamics of plant

populations in salt-desert shrub vegetation grazed by sheep.

Logan: Utah State University. 292 p. Dissertation.

Applegate, C. K. 1996. Allocation of forage among elk and cattle and

vegetative composition of several joint elk-cattle use ranges in

eastern Utah. Provo, UT: Brigham Young University. 66 p. Thesis.

Barrow, J. R.; McArthur, E. D.; Sosebee, R. E.; Tausch, R. J., comps.

1996. Proceedings: shrubland ecosystem dynamics in a changing

environment; 1995 May 23–25; Las Cruces, NM. Gen. Tech. Rep.

INT-GTR-338. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station. 275 p.

Beck, J. L. 1996. Elk and domestic sheep interactions in an aspendominated ecosystem: use of, and impact on vegetation, habitat,

and minerals, as well as implications for ecosystem management.

Provo, UT: Brigham Young University. 396 p. Thesis.

Beck, J. L.; Flinders, J. T.; Nelson, D. R.; Clyde, C. L. 1996a. Dietary

overlap and preference of elk an domestic sheep in aspen-dominated habitats in north-central Utah. In: Evans, K. E., comp.

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a livestock/big game symposium; 1996 February 26–28; Sparks,

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of Agriculture, Forest Service, Intermountain Research Station:

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Beck, J. L.; Flinders, J. T.; Nelson, D. R.; Clyde, C. L.; Smith, H. D.;

Hardin, P. J. 1996b. Elk and domestic sheep interaction in a

north-central Utah aspen ecosystem. Res. Pap. INT-RP-491.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Research Station. 114 p.

Beckstead, J.; Meyer, S. E.; Allen, P. S. 1996. Bromus tectorum seed

germination: between-population and between-year variation.

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Belnap, J. 1996. Soil surface disturbances in cold deserts: effects on

nitrogenase activity in cyanobacterial-lichen soil crusts. Biology

and Fertility of Soils. 23: 362–367.

Buttars, S. M. 1996. Pelletized cyanobacterial soil amendments:

laboratory testing for survival, escapability, and nitrogen fixation. Provo, UT: Brigham Young University. 43 p. Thesis.

Christensen, M.; Meyer, S. C.; Allen, P. S. 1996. A hydrothermal

time model of seed after-ripening in Bromus tectorum L. Seed

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UT: Utah Division of Wildlife Resources, Shrub Sciences Laboratory. 348 p.

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Department of Agriculture, Forest Service, Intermountain Research Station: 178–181.

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Alados, C. L. 1996. Developmental instability as a bioindicator of

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Department of Agriculture, Forest Service, Intermountain Research Station: 170–177.

Garvin, S. C.; Meyer, S. E.; Carlson, S. L. 1996. Seed germination

studies in Atriplex confertifolia (Torr. & Frem.) Wats. In: Barrow,

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Harper, K. T.; Van Buren, R.; Kitchen, S. G. 1996. Invasion of alien

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ranges, and watersheds in the Northern Rocky Mountains: a

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Kitchen, S. G.; Monsen, S. B. 1996. Arrowleaf balsamroot

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Liao, J. 1996. Phenological development and seed germination

characteristics of rush skeltonweed in southwestern Idaho. Provo,

UT: Brigham Young University. 57 p. Thesis.

McArthur, E. D.; Monsen, S. B. 1996. Great Basin Experimental

Range. In: Schmidt, W. C.; Friede, J. L., comps. Experimental

forests, ranges, and watersheds in the Northern Rocky Mountains:

a compendium of outdoor laboratories in Utah, Idaho, and Montana. Gen. Tech. Rep. INT-GTR-334. Ogden, UT: U.S. Department

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McArthur, E. D.; Ott, J. E. 1996. Potential natural vegetation in the

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McArthur, E. D.; Sanderson, S. C. 1996. Twist Hollow: a Mojave

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sustainable biosphere, proceedings of the Fifth International

Rangeland Congress; 1995 July 23–28; Salt Lake City, UT.

Volume 1. Denver, CO: Society for Range Management: 350–351.

McArthur, E. D.; Sanderson, S. C.; Davis, J. N. 1996. Adaptation of

forage kochia accessions across an environmental gradient in

Rush Valley, Utah. Arid Soil Research and Rehabilitation. 10:

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Messina, F. J.; Richards, J. H.; McArthur, E. D. 1996. Variable

responses of insects to hybrid versus parental sagebrush in

common gardens. Oecologia. 107: 513–521.

Meyer, S. E. 1996. Native versus native: an ecologist’s perspective.

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Monaco, T. A. 1996. Use of dark respiration to determine optimal

adaptability in native Great Basin plant species. Provo, UT:

Brigham Young University. 74 p. Thesis.

Monaco, T. A.; Smith, B. N.; Hemming, D.; Hansen, L. D.; Monsen,

S. B.; Carlson, S. L. 1996. Dark respiration comparisons of forbs

and grasses from common gardens. In: Barrow, J. R.; McArthur,

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23–25; Las Cruces, NM. Gen. Tech. Rep. INT-GTR-338. Ogden,

UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station: 210–213.

Monsen, S. B.; Shaw, N. L. 1996. Interseeding fourwing saltbush

(Atriplex canescens) with crested wheatgrass (Agropyron

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Monsen, S. B.; Stevens, R.; Walker, S. C. 1996. The competitive

influence of seeded smooth brome (Bromus inermis) and intermediate wheatgrass (Thinopyron intermedium) within aspen-mountain brush communities of central Utah. In: West, N. E., ed.

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Pendleton, R. L.; Nelson, S. D.; Rodriquez, R. L. 1996. Do soil factors

determine the distribution of spineless hopsage (Grayia brandgei)?

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Pendleton, R. L.; Warren, S. D. 1996. Effects of cryptobiotic soil

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Atriplex. Provo, UT: Brigham Young University. 113 p. Dissertation.

Stevens, R.; Jorgensen, K. R.; Young, S. A.; Monsen, S. B. 1996. Forb

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Tiedemann, A. R.; Clary, W. P. 1996. Nutrient distribution in

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Walker, S. C.; Mann, D. K.; McArthur, E. D. 1996. Plant community

changes over 54 years within the Great Basin Experimental

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Wang, Z. 1996. Ecological analysis of a stable hybrid zone between

two big sagebrush subspecies (Artemisia tridentatassp. tridentata

and A. t. ssp. vaseyana) in Utah. Detroit, MI: Wayne State

University. 132 p. Dissertation.

Welch, B. L. 1996. Effects of humidity on storing big sagebrush seed.

1996. Res. Pap. INT-RP-493. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Research Station. 5 p.

Welch, B. L.; Briggs, S. F.; Johansen, J. H. 1996. Big sagebrush seed

storage. Res. Note INT-RN-430. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Research Station. 3 p.

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Currans, S. P.; Kitchen, S. G.; Lambert, S. M. 1997. Ensuring

identity and quality of native seeds. In: Shaw, N. L.; Roundy, B.

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Freeman, D. C.; Lovett Doust, J.; El-Keblawy, A.; Miglia, K. J.;

McArthur, E. D. 1997. Sexual specialization and inbreeding

avoidance in the evolution of dioecy. Botanical Review. 63: 65–92.

Jones, A. R. 1997. Calorimetric studies of stress effects on the

respiration and growth of radish, small burnet, and alfalfa.

Provo, UT: Brigham Young University. 74 p. Thesis.

Meyer, S. E. 1997a. Arctomecon. In: Flora of North America, North

of Mexico, Volume 3. New York: 312–313.

Meyer, S. E. 1997b. Ecological correlates of achene mass variation

in Chrysothamnus nauseosus (Asteraceae). American Journal of

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Meyer, S. E.; Allen, P. S.; Beckstead, J. 1997. Seed germination

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June 8–19; Winnepeg, Manitoba and Saskatoon, Saskatchewan,

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Randall, P. F. 1997. Sex determination in dioecous species of

Atriplex L. Provo, UT: Brigham Young University. 48 p. Thesis.

Stevens, A. R. 1997. Squirreltail (Elymus elymoides) establishment

and competition with cheatgrass (Bromus tectorum). Provo, UT:

Brigham Young University. 57 p. Dissertation.

Stutz, H. C.; Chu, G-L.; Sanderson, S. C. 1997. Atriplex erecticaulis

(Chenopodiaceae): a new species from south-central California.

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Tew, R. K.; Kitchen, S. G.; Holmgren, R. C. 1997. Soil survey—

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Tiedemann, A. R.; Lambert, S. M.; Carlson, J. R.; Perry, C. J.; Shaw,

N. L.; Welch, B. L.; Driver, C. H. 1997. ‘Umatilla’ snow buckwheat

for rangeland restoration in the Interior Pacific Northwest.

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Upper Colorado Environmental Plant Center; U.S. Department of

Agriculture, Natural Resources Conservation Service; U.S. Department of Agriculture, Forest Service, Intermountain Research Station; Colorado Agricultural Experiment Station. 1997.

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tridentata as a unique low-growing ecotype for wildlife and

rangeland use. Meeker, CO: Upper Colorado Environmental

Plant Center. 5 p.

Wang, H.; McArthur, E. D.; Sanderson, S. C.; Graham, J. H.;

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UT. Proc. RMRS-P-11. Ogden, UT: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station: 171–174.

2000

Allen, P. S.; Meyer, S. E.; Kahn, M. A. 2000. Hydrothermal time as

a tool in comparative germination studies. In: Black, M.; Bradford,

K. J.; Vázzques-Ramos, J., eds. Seed biology; advances and

applications. Cambridge, United Kingdom: University Press:

401–410.

Davis, J. N.; Farmer, M. E.; Green, A. D. 2000a. Utah big game range

trend studies, 1999, volume 1. Publ. 00-01. Provo, UT: Utah

Division of Wildlife Resources, Shrub Sciences Laboratory. 574 p.

Davis, J. N.; Farmer, M. E.; Green, A. D. 2000b. Utah big game range

trend studies, 1999, volume 2. Publ. 00-02. Provo, UT: Utah

Division of Wildlife Resources, Shrub Sciences Laboratory. 609 p.

Green, Ashley D. 2000. A comparison of small mammal abundance,

richness, and diversity in relation to habitat variables in chained

and native pinyon-juniper woodlands. Provo, UT: Brigham Young

University. 42 p. Thesis.

Kitchen, S. G.; Meyer, S. E.; Walker, S.; Wilson, G. R. 2000a. Rule

change proposal no. 3: to amend instructions for paired tests to

include non-woody species and multiple prechill treatments. The

Seed Technologist Newsletter. 74(1): 79–80.

Kitchen, S. G.; Meyer, S. E.; Walker, S.; Wilson, G. R. 2000b. Rule

change proposal no. 4: addition of Penstemon eatonii—firecracker penstemon and Penstemon palmerii—Palmer penstemon to table 1 of the rules. The Seed Technologist Newsletter.

74(1): 81–83.

Leidolf, A.; Wolfe, M. L.; Pendleton, R. L. 2000. Bird communities of

Gambel oak: a descriptive analysis. Gen. Tech. Rep. RMRS-GTR48. Fort Collins, CO: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station. 30 p.

Liao, J. D.; Monsen, S. B.; Anderson, V. J.; Shaw, N. L. 2000. Seed

biology of rush skeltonweed in sagebrush steppe. Journal of

Range Management. 53: 544–549.

McArthur, E. D. 2000. Sagebrush systematics and distribution. In:

Entwistle, P. G.; DeBolt, A. M.; Kaltenecker, J. H.; Steenholf, K.,

comps. Proceedings: sagebrush steppe ecosystem symposium;

1999 June 23–25; Boise, ID. BLM/ID/PT-001001+1150. Boise, ID:

U.S. Department of the Interior, Bureau of Land Management,

Idaho State Office: 9–14.

McArthur, E. D.; Kitchen, S. G.; Uresk, D. W.; Mitchell, J. E. 2000.

Applicability of Montreal process criterion 2—productive capacity—to rangeland sustainability. International Journal of Sustainable Development and World Ecology. 7: 97–106.

Medin, D. E.; Welch, B. L.; Clary, W. P. 2000. Bird habitat relationships along a Great Basin elevational gradient. Res. Pap. RMRSRP-23. Fort Collins, CO: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station. 22 p.

Meyer, S. E.; Debaene-Gill, S. B.; Allen, P. S. 2000a. Using hydrothermal time concepts to model seed germination response to

temperature, dormancy loss, and priming effects in Elymus

elymoides. Seed Science Research. 10: 213–223.

Meyer, S. E.; Nelson, D. L.; Clement, S.; Paulsen, A. 2000b. Exploring the potential for biocontrol of cheatgrass with the headsmut

pathogen. In: Entwistle, P. G.; DeBolt, A. M.; Kaltenecker, J. H.;

Steenholf, K., comps. Proceedings: sagebrush steppe ecosystem

symposium; 1999 June 23–25; Boise, ID. BLM/ID/PT001001+1150. Boise, ID: U.S. Department of the Interior, Bureau

of Land Management, Idaho State Office: 70-72.

Meyer, S. E.; Paulsen, A. 2000. Chilling requirements for seed germination of 10 Utah species of perennial wild buckwheat (Eriogonum

Michx. [Polygonaceae]). Native Plants Journal. 1: 18–24.

Meyer, S. E.; Pendleton, R. L. 2000. Genetic regulation of seed

dormancy in Purshia tridentata (Roseaceae). Annals of Botany.

85: 521–529.

Monsen, S. B. 2000. Establishment of big sagebrush (Artemisia

tridentata) in semiarid environments. In: Entwistle, P. G.; DeBolt,

A. M.; Kaltenecker, J. H.; Steenholf, K., comps. Proceedings:

sagebrush steppe ecosystem symposium; 1999 June 23–25; Boise,

ID. BLM/ID/PT-001001+1150. Boise, ID: U.S. Department of the

Interior, Bureau of Land Management, Idaho State Office: 81–86.

Monsen, S. B.; Shaw, N. L. 2000. Big sagebrush (Artemisia tridentata)

communities—ecology, importance and restoration potential. In:

2000 Billings land reclamation symposium; 2000 March 20–24,

Billings, MT. Reclamation Research Unit Publ. 00-01. Bozeman:

Montana State University: 255–270.

Pendleton, R. L. 2000. Pre-inoculation by an arbuscular mycorrhizal

fungus enhances male reproductive output of Cucurbita

foetidissima. International Journal of Plant Science. 161: 683–689.

Pendleton, R. L.; Pendleton, B. K.; Howard, G. L. 2000a. Effects of

microbiotic soil crust organisms and mycorrhizal fungi on seedling growth of blackbrush (Colegyne ramosissima). CERL Tech.

Rep. 99/108. Champaign, IL: Department of the Army, Construction Engineering Research Laboratory, Corps of Engineers. 26 p.

Pendleton, R. L.; Freeman, D. C.; McArthur, E. D.; Sanderson, S. C.

2000b. Gender specialization in heteodichogamous Grayia

brandegie (Chenopodiaceae): evidence for an alternative pathway to dioecy. American Journal of Botany. 87: 508–516.

Shaw, N. L.; Monsen, S. B. 2000. Controlling annual grasses with

Oust® herbicide. In: Entwistle, P. G.; DeBolt, A. M.; Kaltenecker,

J. H.; Steenholf, K., comps. Proceedings: sagebrush steppe ecosystem symposium; 1999 June 23–25; Boise, ID. BLM/ID/PT001001+1150. Boise, ID: U.S. Department of the Interior, Bureau

of Land Management, Idaho State Office: 66–69.
40 USDA Forest Service Proceedings RMRS-P-21. 2001

McArthur The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective

Sherwin, R. E.; Stricklan, D.; Rogers, D. S. 2000. Roosting affinities

of Townsend’s big-eared bat (Corynorhinus townsendii) in northern Utah. Journal of Mammalogy. 81: 939–947.

Vernon, J. L. 2000. The response of native species after two-way

chaining and seeding in Utah. Provo, UT: Brigham Young University. 49 p. Thesis.

Appendix B: Reports ____________

These are unpublished reports on file at the Shrub Sciences Laboratory documenting extramural research agreements. These documents are not included in the table 2

totals.

Beck, J. L.; Flinders, J. T.; Smith, H. D. 1995. Ecosystem management in relationship to elk and domestic sheep interactions in

aspen-dominated habitat: Willow Creek Demonstration Area,

Uinta National Forest; final research report. Provo, UT: Brigham

Young University. Submitted to U.S. Department of Agriculture,

Forest Service, Uinta National Forest and Central Region, Utah

Division of Wildlife Resources, Provo, UT. 380 p.

Harper, K. T.; McArthur, E. D.; Sanderson, S. C.; Tuhy, J. 1993.

Final report: Zion National Park vegetation summary. Provo, UT:

Brigham Young University. Submitted to U.S. Department of the

Interior, National Park Service, Zion National Park, UT. 246 p.

Haws, B. A. 1991. Final technical report for Project 22-c-6-INT-124,

the role of insects in causing the recent widespread dieoff of

wildland range shrubs, and technical report for Project INT872821, incidence, biology and relationship of the shadscale

mealybug to widespread shrub death. Logan, UT: Department of

Biology, Utah State University. Submitted to U.S. Department of

the Interior, Bureau of Land Management, Utah State Office,

Salt Lake City, UT. 344 p.

Kitchen, S. G. 1997. An investigation of seed dormancy and germination requirements for needle-and thread (Stipa comata); a progress

report submitted to the Association of Official Seed Analysts

(AOSA) Seed Testing Standardization Research Funding Committee. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Shrub Sciences Laboratory. 6 p.

Kitchen, S. G. 1998. An investigation of seed dormancy and germination requirements in four globemallow (Sphaeralcea) species; a

progress report submitted to the Association of Official Seed

Analysts (AOSA) Seed Testing Standardization Research Funding

Committee. U.S. Department of Agriculture, Forest Service, Rocky

Mountain Research Station, Shrub Sciences Laboratory. 4 p.

Kitchen, S. G.; Meyer, S. E. 1999. Seed dormancy and germination

requirements for three Eriogonum (wild buckwheat) species; a

progress report submitted to the Association of Official Seed

Analysts (AOSA) Seed Testing Standardization Research Funding

Committee. U.S. Department of Agriculture, Forest Service, Rocky

Mountain Research Station, Shrub Sciences Laboratory. 5 p.

Kitchen, S. G.; Meyer, S. E.; Walker, S. C. 1999. Development of

standards and rules for testing seed quality of plant species used

in range and wildlands rehabilitation; a progress report for

contract #97-0635 for the Utah Department of Agriculture and

Food. U.S. Department of Agriculture, Forest Service, Rocky

Mountain Research Station, Shrub Sciences Laboratory. 12 p.

Kitchen, S. G.; Stevens, R. 1997. Development of standards and

rules for testing seed quality of plant species used in range and

wildlands rehabilitation, a final report for contract #97-0635 for

the Utah Department of Agriculture and Food. U.S. Department

of Agriculture, Forest Service, Rocky Mountain Research Station, Shrub Sciences Laboratory. 9 p.

Kitchen, S. G.; Stevens, R.; Walker, S. C. 1998. Development of

standards and rules for testing seed quality of plant species

used in range and wildlands rehabilitation, a progress report

for contract #97-0635 for the Utah Department of Agriculture

and Food. U.S. Department of Agriculture, Forest Service,

Rocky Mountain Research Station, Shrub Sciences Laboratory. 11 p.

McArthur. E. D. 1992. Final report: MIPR 92-248. Propagation

and biology of cryptobiotic crusts. Provo, UT: U.S. Department

of Agriculture, Forest Service, Intermountain Research Station, Shrub Sciences Laboratory. Submitted to Construction

Engineering Laboratory, U.S. Army Corp of Engineers,

Champaign-Urbana, IL. 133 p.

McArthur, E. D.; Blauer, A. C.; Monsen, S. B. 1986. Final report:

history of and rehabilitation recommendations for sites disturbed

by modern man’s activities in Grand Teton National Park. Provo,

UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station, Shrub Sciences Laboratory. Submitted to

U.S. Department of the Interior, National Park Service, Grand

Teton National Park, WY. 46 p.

McArthur, E. D.; Pendleton, R. L.; Pendleton, B. K. 1993. Final

report: MIPR E5292N159, propagation and biology of cryptobiotic

crusts 93. U.S. Department of Agriculture, Forest Service, Intermountain Research Station, Shrub Sciences Laboratory. Submitted to Construction Engineering Laboratory, U.S. Army Corp of

Engineers, Champaign-Urbana, IL. 144 p. + video.

McArthur, E. D.; Pendleton, R. L.; Pendleton, B. K. 1995. Final

report: MIPR 94N077, microphytic crust biology and propagation. U.S. Department of Agriculture, Forest Service, Intermountain Research Station, Shrub Sciences Laboratory. Submitted to

Construction Engineering Laboratory, U.S. Army Corp of Engineers, Champaign-Urbana, IL. 145 p.

McArthur, E. D.; Sanderson, S. C. 1992. Final report: desert

tortoise habitat studies. Interagency agreement INT-89402-IA

(UT-910-IA-87). Provo, UT: U.S. Department of Agriculture,

Forest Service, Intermountain Research Station, Shrub Sciences Laboratory. Submitted to U.S. Department of the Interior, Bureau of Land Management, Utah State Office, Salt Lake

City, UT. 388 p.

McArthur, E. D.; Sanderson, S. C. 1992. Final report: vegetation

patterns: 1960–1990, Great Sand Dunes National Monument,

Interagency Agreement 1268-19105, Project Number GRRSARR91-0170. Provo, UT: U.S. Department of Agriculture, Forest Service, Intermountain Research Station, Shrub Sciences

Laboratory. Submitted to U.S. Department of the Interior,

National Park Service, Rocky Mountain Regional Office, Denver, CO. 262 p.

Monsen, S. B.; Kitchen, S. G. 1990. Annual report 1990: a summary

of activities and progress corresponding to Interagency Agreement Number ID910-IA8-04: U.S. Department of Agriculture,

Forest Service, Intermountain Research Station, Shrub Sciences

Laboratory, Provo, UT. Submitted to U.S. Department of the

Interior, Bureau of Land Management, Idaho State Office, Boise,

ID. 17 p.

Monsen, S. B.; Kitchen, S. G. 1991. Annual report 1991: a summary

of activities and progress corresponding to Interagency Agreement Number ID910-IA8-04: U.S. Department of Agriculture,

Forest Service, Intermountain Research Station, Shrub Sciences

Laboratory, Provo, UT. Submitted to U.S. Department of the

Interior, Bureau of Land Management, Idaho State Office, Boise,

ID. 34 p.

Monsen, S. B.; Kitchen, S. G. 1992. Annual report 1992: a summary

of activities and progress corresponding to Interagency Agreement Number ID910 between USDI, Bureau of Land Management and USDA, Forest Service, Intermountain Research Station: U.S. Department of Agriculture, Forest Service,

Intermountain Research Station, Shrub Sciences Laboratory,

Provo, UT. Submitted to U.S. Department of the Interior, Bureau

of Land Management, Idaho State Office, Boise, ID. 62 p.

Monsen, S. B.; Kitchen, S. G. 1993. Annual report 1993: summary

report of progress related to Interagency Agreement Number

ID910 between USDI, Bureau of Land Management and USDA,

Forest Service, Intermountain Research Station: U.S. Department of Agriculture, Forest Service, Intermountain Research

Station, Shrub Sciences Laboratory, Provo, UT. Submitted to

U.S. Department of the Interior, Bureau of Land Management,

Idaho State Office, Boise, ID. 41 p.

Monsen, S. B.; Kitchen, S. G. 1994. Annual report 1994: summary

report of progress related to Interagency Agreement Number

ID910 between USDI, Bureau of Land Management and USDA,

Forest Service, Intermountain Research Station: U.S. Department of Agriculture, Forest Service, Intermountain Research

Station, Shrub Sciences Laboratory, Provo, UT. Submitted to

U.S. Department of the Interior, Bureau of Land Management,

Idaho State Office, Boise, ID. 45 p.

Monsen, S. B.; Kitchen, S. G.; Shaw, N. L.; Naillon, D. G. 1995.

Progress report 1995: Interagency Agreement Number ID910
USDA Forest Service Proceedings RMRS-P-21. 2001 41

The Shrub Sciences Laboratory at 25 Years: Retrospective and Prospective McArthur

between USDI, Bureau of Land Management and USDA, Forest

Service, Intermountain Research Station: U.S. Department of

Agriculture, Forest Service, Intermountain Research Station,

Shrub Sciences Laboratory, Provo, UT. Submitted to U.S. Department of the Interior, Bureau of Land Management, Idaho

State Office, Boise, ID. 39 p.

Monsen, S. B.; Kitchen, S. G.; Shaw, N. L.; Naillon, D. G. 1996.

Annual report 1996: Summary report of progress related to

Interagency Agreement Number ID910 between USDI, Bureau

of Land Management and USDA, Forest Service, Intermountain

Research Station: U.S. Department of Agriculture, Forest Service, Intermountain Research Station, Shrub Sciences Laboratory, Provo, UT. Submitted to U.S. Department of the Interior,

Bureau of Land Management, Idaho State Office, Boise, ID. 52 p.

Monsen, S. B.; Naillon, D., Memmott, K. L.; Kitchen, S. G.;

Carlson, S. L. 1998. Intermountain Greenstrip Research Project,

cooperative research studies, Agreement number ID910: U.S.

Department of Agriculture, Forest Service, Rocky Mountain

Research Station, Shrub Sciences Laboratory, Provo, UT, 1989–

1998 and U.S. Department of the Interior, Bureau of Land

Management, Idaho State Office. Submitted to U.S. Department of the Interior, Bureau of Land Management, Idaho State

Office, Boise, ID. 285 p.

Nelson, D. L. 1990. Studies on a wildland shrub dieoff occurring in

the Great Basin 1983–1985. A report on a cooperative research

project between U.S. Department of Agriculture, Bureau of Land

Management, Utah State Office; U.S. Department of Agriculture,

Forest Service, Intermountain Research Station, Shrub Sciences

Laboratory; Utah State University; Brigham Young University;

Utah Department of Agriculture; and Utah Division of Wildlife

Resources. Provo, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Research Station, Shrub Sciences Laboratory. Submitted to U.S. Department of the Interior, Bureau of

Land Management, Utah State Office, Salt Lake City, UT. 106 p.

Ott, J. E.; McArthur, E. D.; Sanderson, S. C. 1998. Fire rehabilitation monitoring of BLM lands affected by 1996 fires: a preliminary report of interagency agreement J910A70026. Provo, UT:

U.S. Department of Agriculture, Forest Service, Intermountain

Research Station, Shrub Sciences Laboratory. Submitted to U.S.

Department of the Interior, Bureau of Land Management, Utah

State Office, Salt Lake City, UT. 50 p.

Ott, J. E.; McArthur, E. D.; Sanderson, S. C. 1999. Fire rehabilitation monitoring of BLM lands affected by 1996 fires: second year

report of interagency agreement J910A70026. Provo, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Research Station, Shrub Sciences Laboratory. Submitted to U.S.

Department of the Interior, Bureau of Land Management, Utah

State Office, Salt Lake City, UT. 48 p.

Pendleton, R. L.; Pendleton, B. K. 1995. Final report: MIPR

W2V5AA51113582 microphytic crust biology. U.S. Department

of Agriculture, Forest Service, Intermountain Research Station,

Shrub Sciences Laboratory. Submitted to Construction Engineering Laboratory, U.S. Army Corp of Engineers, ChampaignUrbana, IL. 32 p.

Pendleton, R. L.; Pendleton, B. K. 1996. Final report: MIPR

W52EU260390969 benefit of microphytic crust inoculation and

arbuscular mycorrhizal fungi on productivity of VAM-dependent

forbs. U.S. Department of Agriculture, Forest Service, Intermountain Research Station, Shrub Sciences Laboratory. Submitted to Construction Engineering Laboratory, U.S. Army Corp of

Engineers, Champaign-Urbana, IL. 67 p.

Pendleton, R. L.; Garvin, S. C.; Pendleton, B. K. 1998. Final Report:

MIPR W52EU270930412 microphytic crust biology: evaluation

algal inoculation effectiveness. U.S. Department of Agriculture,

Forest Service, Intermountain Research Station, Shrub Sciences

Laboratory. Submitted to Construction Engineering Laboratory,

U.S. Army Corp of Engineers, Champaign-Urbana, IL. 34 p.

Thacker, R. K.; Flinders, J. T.; Blackwell, B. H.; Smith, H. D. 1995.

Comparison and use of four techniques for censusing three

subspecies of kit fox; a cooperative contract study between Wildlife Section, Utah Division of Wildlife Resources, Brigham Young

University. Submitted to Utah Division of Wildlife Resources,

Salt Lake City, UT. 71 p.
42 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Daniel J. Fairbanks is a Professor in the Department of Botany and Range

Science, Brigham Young University, Provo, UT 84602.

A Century of Genetics

Daniel J. Fairbanks

Abstract—In 1866, Gregor Mendel published his experiments on

heredity in the garden pea (Pisum sativum). The fundamental

principles of inheritance derived from his work apply to nearly all

eukaryotic species and are now known as Mendelian principles.

Since 1900, Mendel has been recognized as the founder of genetics.

In 1900, three botanists, Carl Correns, Hugo De Vries, and Erich

Tschermack von Seysenegg, had independently completed experiments that were similar to Mendel’s, although much less extensive.

When searching the literature, all three encountered Mendel’s

paper and realized that he had described the principles of inheritance and the experimental data to confirm them 34 years earlier.

With their rediscovery, the science of genetics was born in 1900

along with the 20th century. William Bateson coined the term

“genetics” and was the person most responsible for establishing the

new science in the first decade of the 20th century. Thomas Hunt

Morgan and his students established the chromosomal basis of

heredity beginning in 1910. During the 1920s and 1930s, classical

genetics was established, and eugenics became very popular among

the more educated and wealthy members of society. Laws mandating sterilization of perceived unfit people were passed and carried

out. By the late 1930s, Nicolai Vavilov had published his theory of

centers of origin for cultivated plants and established a gene bank

for his collections in Leningrad. During the siege of Leningrad in

1941–1942, nine of his coworkers chose to die of starvation rather

than sacrifice the seeds and tubers that Vavilov had collected. In the

meantime, Vavilov was imprisoned for his opposition to Lysenkoism. He soon died in prison of maltreatment. In the mid-1940s,

George Beadle and Edward Tatum discovered the relationship

between genes and enzymes, and Oswald Avery and his coworkers

discovered that DNA is the genetic material of a bacterial species.

In the early 1950s, Alfred Hershey and Martha Chase discovered

that DNA is the genetic material of a bacteriophage. Shortly after

this time, in 1953, James Watson and Francis Crick determined the

structure of DNA based on evidence collected in several laboratories. Cracking the genetic code became one of the next priorities, a

task that was completed in the 1960s. During the 1970s, recombinant DNA was made, an event that led to molecular applications in

genetics and genetic engineering. The first genetically engineered

pharmaceuticals soon followed. The 1970s and 1980s saw the

development of efficient methods for DNA sequencing, which ultimately led to whole genome sequencing. The first bacterial genome

was sequenced in 1995, the Brewer’s yeast genome in 1996, and the

Drosophila, Arabidopsis, and human genomes in 2000. Fittingly,

the sequencing of the human genome, one of the greatest accomplishments in genetics, came at the 100th birthday of the science of

genetics.

In the year 2000, the science of genetics celebrated its

100th anniversary. In the spring and early summer of 1900,

three botanists, Hugo de Vries, Carl Correns, and Erich von

Tschermack, reported their simultaneous and independent

rediscovery of Mendel’s principle of segregation, an event

that sparked the rapid establishment of genetics as a new

and important science. This paper highlights just a few of

the major events that have made genetics one of the most

powerful and rapidly progressing sciences.

Although genetics entered mainstream science rather

suddenly in 1900, it traces its origin to the mid-1800s with

the experiments of Gregor Mendel. In 1843, Mendel entered

the St. Thomas monastery in the city of Brno, now in the

Czech Republic, and was soon appointed as a seventh-grade

science teacher. He failed his teacher certification examination, an event that prompted the abbot of the monastery to

send him to the University of Vienna. While at the University, Mendel was enamored with the teachings of his botany

professor, Dr. Franz Unger, who, even though Darwin’s

Origin of Species had not yet been published, focused his

teachings on the evolution of species over long periods of

geological time. During the time that Mendel was a student,

Unger wrote an article in which he wrote this remarkable

passage that foreshadowed Mendel’s work: “Who can deny

that new combinations arise out of this permutation of

vegetation, always reducible to certain law-combinations,

which emancipate themselves from the preceding characteristics of the species and appear as a new species” (Orel 1996).

Unger’s teachings infuriated the local clergy who attempted

to have him dismissed. Among the most vocal was Dr. Sebastian

Brunner who wrote of Unger as “a man who openly denied the

Creation and the Creator” and as one of the “professors at socalled Catholic Universities [who] deliver lectures on really

beastly theories for years on end” (Olby 1985). Ironically

Mendel was a devout member of the clergy, but he appears to

have sided with Unger. Mendel wrote of his own work as “the

only right way by which we can finally reach the solution of a

question the importance of which cannot be overestimated in

connection with the history of the evolution of organic forms”

(Stern and Sherwood 1966).

In 1852, Mendel began experiments with pea hybrids that

would last for 8 years. From the scientific literature that he

had read extensively he already knew of the concept of

dominance in peas for four of the seven traits he studied. His

contribution was his development of a mathematical model

to explain heredity. He discovered regular 3:1 ratios in the

F2 generations in all seven of his monohybrid experiments,

and developed the now familiar mathematical model to

explain the 3:1 ratio, which he expressed in the following

equation:

 

A

A

A

a

a

A

a

a +++

where the letters in the numerator represent the alleles

contributed by the male parent and those in the denominator
USDA Forest Service Proceedings RMRS-P-21. 2001 43

A Century of Genetics Fairbanks

as the alleles contributed by the female parent. Because the

large A is dominant, three of the four combinations produce

the dominant phenotype and one the recessive. He tested

this model by allowing the F2 plants to self fertilize to

produce F3 offspring. He found that 1⁄3 of the F2 plants with

the dominant phenotype produced offspring with only the

dominant phenotype, and that 2⁄3 produced offspring with

both dominant and recessive phenotypes, precisely as his

model predicted.

He then turned his attention to dihybrid and trihybrid

experiments to ascertain whether the inheritance of one

trait influences the inheritance of another. He discovered

that all seven traits in various combinations of twos and

threes were inherited independently of one another. On

these two discoveries, the mathematical segregation of differing elements and the independent inheritance of traits,

are based the two laws of inheritance attributed to Mendel:

the law of segregation and the law of independent assortment.

Mendel presented his paper in 1865 and had it published

the following year (Mendel 1866). For the next 34 years, no

one, including Mendel, recognized that the laws he discovered applied almost universally to plants, animals, and

humans. His paper was not completely forgotten; it was cited

at least 15 times before 1900. However, it is clear from these

citations that no one recognized its most important points.

Mendel sent reprints with cover letters to several botanists,

including Franz Unger, his former professor, but the only

one to respond was Karl von Nägeli, who carried on correspondence with Mendel over a period of 7 years. Mendel had

initiated studies with the hawkweed, and Nägeli encouraged Mendel to continue with these species. Neither Mendel

nor Nägeli knew that hawkweed was an apomict, and thus

it did not display the patterns of inheritance that Mendel

had observed in peas, and by now in several other species.

Mendel died in 1884, unaware that he would become

known as the founder of genetics. Sixteen years later, in

1900, DeVries working with several plant species, Correns

with peas and maize, and Tschermak with peas, rediscovered Mendel’s principle of segregation and the science of

genetics was born. Two of the three rediscoverers, Correns

and Tschermak, became strong advocates of Mendelism. De

Vries, on the other hand, dismissed Mendelian inheritance

within less than a year of his paper on it. The person most

responsible for the establishment of Mendelism was the

British naturalist William Bateson. Bateson read Mendel’s

paper while on a train in 1901 and soon thereafter embraced

Mendelism with the passion of religious zealot. Bateson was

so passionately supportive of Mendelism that De Vries

warned him in a 1902 letter, “I prayed you last time, please

don’t stop at Mendel. I am now writing the second part of my

book which treats crossing, and it becomes more and more

clear to me that Mendelism is an exception to the general

rule of crossing. In no way is it the rule!” (Olby 1985). The

opposition to Mendelism only encouraged Bateson, who,

together with Reginald Punnett and Edith Saunders, found

Mendelian inheritance in many different species. It is to

Bateson that we owe much of our current genetic terminology (including the word “genetics”) and the establishment of

Mendelian genetics as a credible science in the first decade

of the 20th century.

Thomas Hunt Morgan was an American zoologist at

Columbia University who at first rejected both the Mendelian

theory of inheritance espoused by Bateson and the chromosomal theory of inheritance promoted by Edmund Wilson,

also at Columbia. He opted instead for de Vries’ mutation

theory (which differs substantially from our current understanding of mutation). Complaining of the intellectual climate at Columbia, Morgan wrote in 1905 that it was “an

atmosphere saturated with chromosomic acid” (Allen 1978).

He completely reversed his views, however, within 5 years

as he brought Mendelian and chromosomal theories of

inheritance together as a single theory. In 1910 he observed

a white-eyed fruit fly that was to change the direction of his

career and the science of genetics. He discovered that the

white-eye phenotype was associated with inheritance of the

X chromosome.

At first, he was reluctant to conclude that the genes were

actually a part of the chromosome. However, two discoveries

by his students, Alfred Sturtevant and Calvin Bridges, made

it clear that their so-called sex-linked genes must be a

physical part of the X chromosome. Sturtevant, as an undergraduate student in 1911, had a flash of genius when he

realized that genes might be located in a linear fashion on

the chromosome. He gathered up the notebooks with the

data from several of their experiments, and, in his words, “I

went home and spent most of the night (to the neglect of my

undergraduate homework) in producing the first chromosome map” (Sturtevant 1965). He placed five genes on a

linear map and calculated the distances between them

based on the frequencies of crossing over. Bridges discovered

in 1913 that unusual cases of inheritance of mutant sexlinked alleles were associated with nondisjunction of chromosomes. The collective data strongly indicated that genes

were organized in a linear fashion as part of the chromosome. Morgan and three of his students, Sturtevant, Muller,

and Bridges, published in 1915 a landmark book entitled the

Mechanism of Mendelian Heredity (Morgan and others 1915)

in which they summarized all of their evidence that Mendelian and chromosomal theories of inheritance were one and

the same. Bateson rejected the idea, but respected their

work so much that he aptly wrote “not even the most

skeptical of readers can go through the Drosophila work

unmoved by a sense of admiration for the zeal and penetration with which it has been conducted, and for the great

extension of genetic knowledge to which it has led—greater

far than has been made in any one line of work since

Mendel’s own experiments” (Sturtevant 1965).

The students who coauthored this work with Morgan,

Sturtevant, Bridges, and Muller, were to become three of the

most influential geneticists in later years. Another laboratory

was also soon to produce a similar group of prominent geneticists. At Cornell University, Rollins Emerson had taken on

George Beadle, Marcus Rhoads, Charles Burnham, and Barbara McClintock as students to work with him on maize.

McClintock had hoped to study plant breeding, but the Department of Plant Breeding at Cornell did not admit women

at the time, so Emerson invited her to work with him in maize

genetics. McClintock’s enthusiasm for her knowledge is well

illustrated in the following story, given in her words:

I couldn’t wait to take [the final exam for geology]. I loved

the subject so much that I knew they wouldn’t ask me

anything I couldn’t answer. I just knew the course. So I

couldn’t wait to get into the final exam. They gave out these

blue books, to write in and on the front page you put down your
44 USDA Forest Service Proceedings RMRS-P-21. 2001

Fairbanks A Century of Genetics

own name. Well, I couldn’t be bothered with putting my name

down; I wanted to see those questions. I started writing right

away—I was delighted, I just enjoyed it immensely. Everything was fine, but when I got to write my name down, I

couldn’t remember it. I couldn’t remember to save me, and I

waited there. I was much too embarrassed to ask anybody

what my name was, because I knew they would think I was

a screwball. I got more and more nervous, until finally (it took

about twenty minutes) my name came to me.

—Keller (1983)

Although McClintock is best known for her later discovery

of transposable elements in maize, among her most significant publications was her demonstration that chromosomes

were the physical carriers of genes. The work of Morgan and

his students had shown the association of genes and chromosomes, which led them to conclude that genes were on

chromosomes. However, McClintock and her coworker

Harriet Creighton had observed cytological evidence of crossing over that was clearly associated with the recombination

of linked genes in maize. Morgan gave a lecture at Cornell in

1931, and then took a tour of the labs. Creighton and

McClintock showed Morgan their data, which they felt were

rather meager. They had intended to grow their maize

plants another year to collect more data before publishing

the results. Morgan knew of similar work in Drosophila

being conducted by Curt Stern, but did not tell them of it. He

insisted that Creighton and McClintock publish their results immediately. He asked for a pen and paper and in their

presence wrote a letter to the editor of the Proceedings of the

National Academy of Sciences telling him that he would

receive within 2 weeks a significant article from Creighton

and McClintock that should be immediately published. The

article beat Stern’s by several months. Explaining his actions, Morgan simply said, “I thought it was about time that

corn got a chance to beat Drosophila” (Keller 1983).

Like most other sciences, genetics was not immune to

political influences. The eugenic movement gained momentum in the period from turn of the century to the 1930s.

Based on incorrect assumptions about the inheritance of

such traits as feeblemindedness, imbecility, and criminality, antimiscegenation and mandatory sterilization laws

were passed in many states and in several European countries. Before such laws were rescinded, over 60,000 people

suffered involuntary sterilization in the United States. Although many geneticists favored eugenics to some degree,

some of them pointed out the theoretical flaws implicit in

these laws. Morgan in particular renounced his membership

in a society that promoted eugenics, and later in his Nobel

acceptance speech, given in 1935, he stated, “The claims of

a few enthusiasts that the human race can be entirely

purified or renovated at this later date, by proper breeding,

have I think been greatly exaggerated. Rather must we look

to medical research to discover remedial measures to insure

better health and more happiness for mankind” (Morgan

1935). Eugenics reached its most tragic point with the

genocide of millions by the Nazi regime before and during

World War II. Unfortunately, eugenic measures are still

with us. Reports of genocide and ethnic cleansing are still an

atrocious part of our modern world.

Some of the most tragic effects of politics and war on

genetics were in Russia in the 1930s and 1940s. Nicolai

Vavilov was a brilliant Russian plant geneticist who recognized the need to preserve genetic diversity in plants. His

worldwide studies identified the centers of origin and diversity for the major food crops of the world. Vavilov and his

associates collected seeds and tubers of those crops and

created one of the world’s first gene banks in Leningrad. In

the winter of 1941–1942, Hitler’s army laid siege to Leningrad

and food soon ran out. Tens of thousands of the city’s

residents died of starvation. The scientists in the institute

Vavilov had directed were surrounded by stores of rice,

wheat, corn, peanuts, potatoes, and peas that contained the

genetic diversity collected by Vavilov and his associates.

Recognizing the need to preserve that diversity, they made

a pact among themselves that none of them would eat the

seeds and tubers. Nine of the scientists died of starvation

while at their posts in the Institute rather than sacrifice the

genetic diversity that was stored there.

A few years earlier, Vavilov was the most prominent

geneticist in Russia. However, in the 1930s, Trofim Lysenko

began to promote his Lamarckian ideas that the environment could direct specific changes in hereditary elements,

and referred in distaste to Vavilov and his colleagues as “the

dogmatic followers of Mendel and Morgan” (Medvedev 1969).

Vavilov publicly resisted Lysenko, but in the end, Stalin

declared Lysenko’s views as state policy. In 1939, at one of

his last attempts to challenge Lysenko, Vavilov stated his

resolve, “We shall go to the pyre, we shall burn, but we shall

not retreat from our convictions” (Medvedev 1969). Shortly

thereafter, in 1940, Vavilov and several other Soviet geneticists were arrested and imprisoned for their refusal to follow

Lysenko. As Hitler’s army advanced during 1941, Vavilov as

a prisoner was evacuated from St. Petersburg to Saratov

prison and placed in a windowless underground cell called a

death cell. There he died in January 1943, a year after the

deaths of his colleagues in the institute. Numerous Soviet

geneticists were imprisoned and killed because of their

refusal to accept Lysenkoism. Lysenko reigned over Soviet

genetics for nearly 3 decades until 1964 when Khrushchev,

who had firmly supported Lysenko, was forced to resign.

We now return to the United States. In the early 1940s,

George Beadle, one of Emerson’s former students, and Edward Tatum discovered that genes were related to enzymes.

In a sense, they had simply clarified the same concept that

Archibald Garrod and William Bateson had proposed in

1902, but with much more evidence and in much more detail.

The association between genes and proteins was evident,

but their real relationship was yet to be revealed.

Although DNA was discovered by Friedrich Miescher

shortly after Mendel did his work, the connection between

DNA and heredity began to surface about the same time that

Beadle and Tatum demonstrated the association of genes

and proteins. In 1944, Oswald Avery, Colin McLeod, and

Maclyn McCarty found that the hereditary substance of the

bacterium Streptococcus pneumoniae was DNA. In 1952,

Alfred Hershey and Martha Chase demonstrated that the

hereditary material of the bacteriophage T2 was also DNA.

However, even in light of these results, most scientists still

refused to accept DNA as the hereditary substance. According to James Watson, “Al Hershey had sent me a long

letter...summarizing the recently completed experiments by

which he and Martha Chase established that a key feature

of the infection of a bacterium by a phage was injection of

DNA....Their experiment was...a powerful new proof that

DNA is the primary genetic material....Nonetheless, almost
USDA Forest Service Proceedings RMRS-P-21. 2001 45

A Century of Genetics Fairbanks

no one in the audience of over four hundred microbiologists

seemed interested as I read long sections of Hershey’s letter”

(Watson 1969).

The disinterest didn’t last long. In 1953, Watson and

Francis Crick, using data gathered entirely from the experiments of others, deduced the structure of DNA. One of the

chief requirements of the hereditary material was the ability

to self-replicate. At the conclusion of their classic paper, they

penned this now-classic line, “It has not escaped our notice

that the specific pairing we have postulated immediately

suggests a possible copying mechanism for the genetic material” (Watson and Crick 1953).

About this same time, it was clear that DNA somehow

encoded the composition of proteins, and that RNA was an

intermediate between DNA and protein. The relationship

between nucleotide sequence and amino acid sequence was

yet to be established. Through brilliant mathematical analysis by Syndey Brenner, and through analysis of the effect of

mutations on amino acid sequence, geneticists realized that

the genetic code must be nonoverlapping and that three

nucleotides must encode each amino acid. These realizations led Marshall Nirenberg, Heinrich Matthaei, Severo

Ochoa, Philip Leder, Francis Crick, and others to decipher

the genetic code. By 1965, they had identified the amino

acids for 50 of the 64 codons. Then in 1966, the final gaps

were bridged, and the genetic code was revealed.

The genetic code turned out to be nearly universal, an

observation that had profound implications. Because of a

universal code, a gene transferred from one species to another

should encode the same protein in the recipient species as in

the original species. This opened up great possibilities of

genetic engineering, especially with bacteria. In the late

1970s, Goeddel and others (1979) successfully introduced a

cDNA from the human growth hormone gene into Escherichia

coli, and with a little genetic engineering of the promoter and

initiation codon regions, achieved expression of pure human

growth hormone in bacteria. This initiated the age of genetic

pharmacology, which now produces such important human

proteins as insulin, interferon, and clotting factors in bacteria

for medicinal use. So valuable is this industry that the

University of California and Eli Lilly & Co. spent over 30

million dollars in legal fees fighting each other over the patent

for genetically engineered insulin. Lilly won the dispute.

For the most part, the molecular revolution and traditional genetics and breeding remained almost separate

fields. Then in the 1980s came the convergence of the two

with the use of DNA markers to address questions of inheritance and to improve the efficiency of both medical and

agricultural genetics. The 1980s marked the beginning of

genomics. Genetic maps, which before had taken years to

develop, now could be completed sometimes in a period of

weeks. DNA markers overcame the obstacles that had prevented efficient genetic analysis in humans, and the first

saturated human genetic map was completed in 1994.

The ultimate genetic map, however, was the entire nucleotide sequence of a genome. Frederick Sanger, who developed the basic process that is now used in automated

sequencers, reported with colleagues in 1977 the first entire

nucleotide sequence of a genome, that of the phage phi X-174

which consists of 5,386 nucleotide pairs (Sanger and others

1977). It was a huge step from those days to the sequence of

the genome from a cellular organism. Long before the first

bacterial genome was sequenced, the human genome project,

one of the most ambitious undertakings in the history of

science, was begun. To sequence the 3 billion nucleotides of

the human genome, scientists required substantial improvements in laboratory automation and vast cooperation among

many different laboratories. The projected cost of the project

was enormous and it drew significant criticism because

many perceived it as drawing research funding away from

other projects. However, the benefits that came from it,

automated DNA sequencing in particular, have benefited

genetic research in many areas, including much of the

research presented in these proceedings.

In 1995, Craig Venter and his colleagues at the Institute

for Genomic Research published the first genomic sequence

of a cellular organism, that of the bacterium Haemophilus

influenzae with 1,830,137 nucleotide pairs in its genome

(Fleischmann and others 1995). Goffeau and others (1996)

published the first sequence of a eukaryotic genome, that of

Saccharomyces cerevisiae, Brewers yeast, whose genome

contains about 13 million nucleotide pairs and 6,000 genes.

The sequences of numerous bacterial species and that of the

nematode worm Caenorhabditis elegans were also completed. In March 2000, the genomic sequence of Drosophila

melanogaster was published, with 120 million nucleotide

pairs in the euchromatic regions and about 13,600 genes

(Adams and others 2000). Arabidopsis thaliana was the first

plant species to be sequenced (The Arabidopsis Genome

Initiative 2000). Fittingly, at the conclusion of one century of

genetics, the first draft of the human genome was announced, 5 years ahead of schedule.

We have come a long way from Mendel’s garden to the

sequence of the human genome. I’ll resist the temptation to

speculate about what the future holds. One of the delights of

studying the history of genetics is to see how wrong many

authors were when they wrote decades ago about genetics in

our day. This much I feel confident in predicting, however,

that the future of genetics is very bright.

References _____________________

Adams, M. D.; Celniker, S. E.; Holt, R. A.; Evans, C. A.; Gocayne,

J. D.; Amanatides, P. G.; Scherer, S. E.; Li, P. W.; Hoskins, R. A.;

Galle, R. F.; and others. 2000. The genome sequence of Drosophila

melanogaster. Science. 287: 2185–2195.

Allen, G. E. 1978. Thomas Hunt Morgan: The man and his science.

Princeton, NJ: Princeton University Press. 447 p.

Fleischmann, R. D.; Adams, M. D.; White, O.; Clayton, R. A.;

Kirkness, E. F.; Kerlavage, A. R.; Bult, C. J.; Tomb, J.F.; Dougherty,

B. A.; Merrick, J. M.; and others 1995. Whole genome random sequencing and assembly of Haemophilus influenzae. Rd. Science.

269: 496–512.

Goeddel, D. V.; Heyneker, H. L.; Hozumi, T.; Arentzen, R.; Itakura,

K.; Yansura, D. G.; Ross, M. J.; Miozzari, G.; Crea, R.; Seeburg,

P. H. 1979. Direct expression in Escherichia coli of a DNA sequence coding for human growth hormone. Nature 281: 544–548.

Goffeau, A.; Barrell, B. G.; Bussey, H.; Davis, R. W.; Dujon, B.;

Feldmann, H.; Galibert, F.; Hoheisel, J. D.; Jacq, C.; Johnston,

M.; Louis, E. J.; Mewes, H. W.; Murakami, Y.; Philippsen, P.;

Tettelin, H.; Oliver, S. G. Life with 6000 genes. 1996. Science. 274:

546, 563–567.

Keller, E. F. 1983. A feeling for the organism. San Francisco:

W.H. Freeman and Co. 235 p.

Medvedev, Z. A. 1969. The rise and fall of T.D. Lysenko. Trans.

I. M. Lerner. New York, NY: Columbia University Press. 284 p.

Mendel, G. 1866. Versuche über Pflanzen-Hybriden. Verhandl

naturf Verein Brünn 4:3–47.
46 USDA Forest Service Proceedings RMRS-P-21. 2001

Fairbanks A Century of Genetics

Morgan, T. H. 1935. The relation of genetics to physiology and

medicine. Scientific Monthly. 40: 5–18.

Morgan, T. H.; Sturtevant, A. H.; Muller, H. J.; Bridges, C. B. 1915.

The mechanism of Mendelian heredity. New York, NY: Henry

Holt & Co. 262 p.

Olby, R. 1985. Origins of Mendelism, Second Edition. Chicago, IL:

University of Chicago Press. 310 p.

Orel, V. 1996. Gregor Mendel: The first geneticist. Oxford, UK:

Oxford University Press. 353 p.

Sanger, F.; Air, G. M.; Barrell, B. G.; Brown, N. L.; Coulson, A. R.;

Fiddes, C. A.; Hutchison, C. A.; Slocombe, P. M.; Smith, M. 1977.

Nucleotide sequence of bacteriophage phi X174 DNA. Nature.

265: 687–695.

Stern, C.; Sherwood, E. R., eds. 1966. The origin of genetics: A

Mendel source book. San Francisco, CA: W. H. Freeman. 179 p.

Sturtevant, A. H. 1965. A history of genetics. New York, NY: Harper

and Row. 165 p.

The Arabidopsis Genome Initiative. 2000. Analysis of the genome

sequence of the flowering plant Arabidopsis thaliana. Nature.

408: 796–815.

Watson, J. D. 1969. The double helix. New York: Mentor. 143 p.

Watson, J. D.; Crick, F. C. 1953. A structure for deoxyribonucleic

acid. Nature. 171: 737–738.
USDA Forest Service Proceedings RMRS-P-21. 2001 47

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Stephen B. Monsen is a Botanists at the Shrub Sciences Laboratory, Provo,

UT 84606. Nancy L. Shaw is a Botanist at the Forestry Sciences Laboratory,

Boise, ID 83702. Both laboratories are part of the U.S. Department of

Agriculture, Forest Service, Rocky Mountain Research Station.

Development and Use of Plant Resources

for Western Wildlands

Stephen B. Monsen

Nancy L. Shaw

Abstract—Concern for declines in big game habitat throughout the

West and the pioneering work of revegetation researchers in the mid

twentieth century led to increased use of native shrubs, grasses, and

forbs for revegetation, and the 1975 establishment of the U.S.

Department of Agriculture, Forest Service, Shrub Sciences Laboratory in Provo, Utah. During this period revegetation objectives

shifted from an emphasis on production of commodities to conservation of biodiversity and ecosystem functions. Plant resource development altered from an agronomic approach focusing on plant

improvement to one that incorporates ecological, genetic, and practical considerations. Although many problems remain, research,

technological advances, efforts to stabilize the native seed industry,

and improved seed testing and certification procedures are increasing our options for revegetating disturbed lands.

At the 1975 dedication of the Shrub Sciences Laboratory,

the senior author and Donald R. Christensen, then of the

Utah Division of Wildlife Resources, presented a paper

“Woody Plants for Rehabilitating Rangelands in the Intermountain Region” (Monsen and Christensen 1976). This

paper summarized contemporary and anticipated research

needs for the selection and use of native shrubs on disturbed

wildlands, particularly big game ranges. Efforts to improve

habitat for expanding mule deer populations in the Western

States began in the 1940s (McArthur 1992; Plummer and

others 1968). Degradation resulting from abusive livestock

grazing, agricultural development, and urbanization contributed to loss of shrublands that provided important winter and spring/fall ranges for big game (Plummer 1972;

USDA Forest Service 1936). The objective of maintaining

healthy deer herds led to plant materials research that

emphasized the use of shrubs to provide browse and cover.

This effort was led by Federal and university researchers

and western Game and Fish Departments working in cooperation with land management agencies (Plummer and

others 1957; Roundy 1966).

Concern over deteriorating big game ranges in Utah led to

the 1954 initiation of a cooperative program between the

Utah Department of Fish and Game and the U.S. Department of Agriculture, Forest Service, Intermountain Research Station (now the Rocky Mountain Research Station)

that has endured to the present (Blaisdell 1972; McArthur

1992; Roundy and others 1997). Research resulting from

this and similar efforts across the West enabled managers to

begin seeding and planting a variety of shrubs as well as

native and exotic herbaceous understory species to stabilize

disturbances, restore wildlife habitat, and protect watersheds and other rangeland resources (Holmgren and Basile

1959; Hubbard 1962; Hubbard and others 1959; Plummer

1977; Plummer and others 1955, 1968). This research highlighted the importance of recognizing ecotypic variation in

native species and matching plant materials to planting site

conditions and management objectives. Much of the early

work in Utah was summarized in the 1968 publication

“Restoring Big Game Ranges in Utah” (Plummer and others

1968). Progress in Utah led to a greater recognition of

shrubland resources and values (McKell and others 1972)

and the 1975 establishment of the U.S. Department of

Agriculture, Forest Service, Shrub Sciences Laboratory in

Provo (Blaisdell 1972; McArthur 1992; Stutz 1975).

Plant Material Development and

Use, 1912 to 1975 _______________

Shrub revegetation research developed from ongoing efforts to stabilize and restore Western wildlands. Livestock

grazing excesses in the late nineteenth and early twentieth

century negatively impacted vegetation and watershed stability (USDA Forest Service 1936). Massive erosion and

major flood events led to the instigation of research and

management programs to understand the causes of watershed deterioration and implement grazing management

and rehabilitation programs to combat the problem (Forsling

and Dayton 1931; Meeuwig 1960). Initial work begun in

1912 centered on disturbances at upper elevations (Monsen

and McArthur 1995). In the 1920s a research program was

implemented across the Intermountain Region to evaluate

the adaptability and performance of a number of grass, forb,

and shrub species and accessions (Forsling and Dayton

1931; Monsen and McArthur 1995; Plummer and Stewart

1944). Although native species were included in research

studies and field trials from the beginning, exotic grasses

were generally more effective in meeting the criteria of ease

of planting, reliable establishment, rapid production of ground

cover, good palatability and productivity, grazing tolerance,

competitiveness with weeds, good seed quality, and low seed

cost (Monsen and McArthur 1995). A number of introduced

grasses including smooth brome (Bromus inermis Ley.),

intermediate wheatgrass (Elytrigia intermedia [Host]

Nevski), and orchardgrass (Dactylis glomerata L.) were

widely used at mid and upper elevations. Revegetation of

degraded sagebrush rangelands in low precipitation areas

centered on the use of introduced wheatgrasses (Agropyron
48 USDA Forest Service Proceedings RMRS-P-21. 2001

Monsen and Shaw Development and Use of Plant Resources for Western Wildlands

Gaert. spp.). These were seeded on extensive tracts in the

Great Basin and northern shrub steppe during the mid

1900s to improve forage availability for livestock and to

control the spread of halogeton (Halogeton glomeratus [Bieb.]

C.A. Mey.) (Johnson 1986; Mathews 1986; Young and Evans

1986).

Thus, for watershed and livestock plantings, a number of

exotic grasses gained widespread use, while initial poor

showings limited further research with natives (Roundy and

Call 1988). In spite of their apparent effectiveness, problems

posed by exotic grasses eventually became widely recognized. These included the disruption of soil structure and

loss of remnant native species during site preparation for

seeding, lack of diversity and vegetative structure in mature

stands, and susceptibility to insects, disease, and drought

(Box 1986; Pyke 1996). Importantly, exotic grasses often

precluded recovery of natives, and in some cases they were

subject to invasion by weedy species (Elliot and White 1987;

Powell and others 1994; Walker and others 1995). These

limitations, advances in shrub research, and a growing

public concern for conserving ecological values of rangelands

gradually led to increased emphasis on the inclusion of

natives and a greater diversity of species in revegetation

prescriptions. In addition to improvement of big game range,

shrubs and other native species were being recognized as

valuable for low maintenance landscaping, recreation areas,

roadside disturbances, mined lands, and other severely disturbed sites (Blaisdell 1972; Plummer 1972).

For selection of revegetation plant materials, particularly

woody species, researchers emphasized a combination of

approaches used in forest tree seed improvement and techniques utilized in developing agronomic plant varieties

(Plummer 1972). By this time, the wide genetic variability in

terms of ecotypes, biotypes, and chromosome races present

in many intermountain species as a result of past climatic

change and plant migrations was widely recognized (for

example, see Beetle 1960; Stebbins 1950; Stutz and Thomas

1964). Important natural shrub stands were identified for

seed collection, and in some cases, seed orchards from

selected populations of important species were established

(Plummer 1972). Plummer advocated development of geographic ecotypes, selections adapted to specific areas and

exhibiting desirable characteristics. These selections might

represent particular ecotypes or specific plants from an

ecotype, referred to as biotypes or races, that exhibited

desirable characteristics (Plummer 1972). These characteristics were generally related to plant establishment or browse

production and included germinability, seedling vigor, growth

rate, palatability, winter leafiness, and tolerance of browsing (Monsen 1975; Plummer and others 1968).

Many accessions selected for study represented extensive

shrub populations that were regularly harvested by commercial collectors and planted throughout the Intermountain area. Seeds from these stands and collections from

additional populations of interest were widely field tested

for adaptability and performance within and beyond the

current range of the individual populations and species (for

example, see Davis 1983; Edgerton and others 1983; Shaw

and Monsen 1983 for antelope bitterbrush [Purshia tridentata

{Pursh} DC.] and related species). This research ultimately

resulted in the use of a large number of primarily native

shrub species and accessions as well as a variety of native

and exotic grasses and forbs. At the first major wildland

shrub symposium in the Intermountain area, held in Logan,

Utah, in 1971, Blaisdell (1972) reported that extensive

screening and testing of shrubs by the Intermountain Research Station, the Utah Division of Wildlife Resources, and

the Idaho Department of Fish and Game had resulted in the

listing of approximately 75 woody species as promising for

restoration of big game habitats (Plummer and others 1968).

Of this group, about a dozen were most widely planted in

large restoration projects. Four shrubs were considered the

primary species to be investigated and promoted. These

were basin big sagebrush (Artemisia tridentata [Nutt.] ssp.

tridentata), fourwing saltbush (Atriplex canescens [Pursh]

Nutt.), antelope bitterbrush, and rubber rabbitbrush

(Chrysothamnus nauseosus [Pallas] Britt).

Revegetation research fueled further studies of shrubland

ecology and management (for example, see Giunta and

others 1978; Nord 1965; Stevens and others 1977) and

contributed to the expansion of the native seed industry.

Observed variability in intermountain species led to studies

of the genetic and physiological basis for these differences

and contributed to our understanding of the evolution of the

intermountain flora (Blauer and others 1975, 1976;Drobnick

and Plummer 1966; McArthur, this proceedings; McArthur

and others 1979; Stutz and others 1975; Stutz and Thomas

1964). Several seed companies began business in central

Utah and near other centers of revegetation research and

application within the region. Most companies handled both

exotic and native species. Steep slopes and unstable sites

where rapid establishment was critical were often transplanted rather than seeded, providing researchers and Federal, State, and private nurseries the impetus to develop

propagation technology for requested species (Ferguson and

Monsen 1974; Heit 1967, 1968, 1971; Schopmeyer 1974).

Early recognition of the cycle of excessive grazing, creation

of openings in plant communities, invasion by annual weeds,

changes in fire frequency and behavior, and alteration of

secondary succession guided research on the establishment of

wildland plantings (Plummer 1972). Germination, seedling

establishment, and growth data from field trials were used to

develop appropriate planting technologies and prescribe

management and use of young plantings (Basile and Holmgren

1955, 1957; Plummer and others 1968). Existing agricultural

equipment was adapted for harvesting, cleaning, and seeding

the highly varied types of fruits and seeds planted. The

Equipment Development Committee, comprised primarily of

agency and commercial members, was established in 1942 to

address the development of a disk and drill seeder for rangeland conditions (Larson 1982). Development of the Hansen

seed dribbler, interseeders, aerial seeding devices, the anchor

chain, and the rangeland drill enabled land managers to plant

mixtures of potentially competitive species on rugged terrain

(Larson 1982; Vallentine 1989).

Plant Materials Use and Development,

1975 to 2000 ____________________

Federal Land Revegetation Policy

Changes in Federal land management policy during the

twentieth century reflected trends in public concern for the
USDA Forest Service Proceedings RMRS-P-21. 2001 49

Development and Use of Plant Resources for Western Wildlands Monsen and Shaw

condition and sustainability of public land resources and

have directly or indirectly dictated approaches to the selection and use of plant materials. Over this period, policy

shifted from an emphasis on commodity production to facilitation of multiple uses to conservation of biodiversity and

ecosystem management (Davis 1997; Loomis 1993; Richards

and others 1998; Tzoumis 1998). Current guidance for revegetation of Federal lands has evolved over the last 40 years

and generally encourages the use of native species when

feasible or practical (table 1). Additional direction is available for specific agencies and categories of land disturbances

(see below). Land managers planning revegetation efforts

are now attempting to address the scale-associated problems of reestablishing vegetation not only on site-specific

projects but within the context of management at the landscape level (Bell and others 1997; Ehrenfeld and Toth 1997;

Jelinski 1997; Whisenant 1999). Local revegetation policies

and guidelines evolve and are updated more or less continuously (for example, USDA Forest Service 2000a; USDI

Bureau of Land Management 1996). Concerns and conflicts

Table 1—Selected Federal legislation and Executive Orders and Memoranda impacting the selection and use of plant materials, 1960

to present.

Document Year Direction

Multiple Use Sustained Yield 1960 Agencies directed to manage reserved Federal lands for recreation,

Act (P.L. 86-517; U.S.C. 528- watershed values, grazing, timber, fish, and wildlife, thus increasing

531)a the emphasis on noncommercial resources.

Classification and Multiple Use 1964 Agencies directed to manage reserved Federal lands for recreation,

Act (P.L. 88-607; 43 U.S.C. watershed values, grazing, timber, fish, and wildlife, thus increasing

1411-1418)a the emphasis on noncommercial resources.

Wilderness Act (P.L. 88-577; 1964 Provided for designation of wilderness areas to be “preserved and

16 U.S.C. 1131-1136)a protected in their natural condition.”

National Environmental Policy 1969 Federal agencies directed to analyze impacts of proposed disturbances

Act (P.L. 91-190; 42 U.S.C. in environmental assessments and include public participation in

4321 et. seq)a decisionmaking.

Forest and Rangeland Renewable 1974 Federal agencies required to assess use and availability of natural

Resources Planning Act (P.L. 93- resources on Federal lands and develop management direction for

378; 16 U.S.C. 1610-1616)a National Forests.

National Forest Management Act 1976 Directed National Forests to submit management plans every 5 years.

(P.L. 94-588; 16 U.S.C. 1600-1616)a

Federal Land Policy and 1976 Prescribed BLM response to the Resources Planning Act. Required

Management Act (P.L. 94- planning to protect biodiversity, designate wilderness study areas,

579; 43 U.S.C. 1701 et. seq.)a and control extraction of locatable minerals.

Endangered Species Act (P.L. 1973 Responsibility for managing endangered species and their habitat

93-205; U.S.C. 1531-43)a transferred from the States to the U.S. Department of the Interior,

Fish and Wildlife Service.

Executive Order 11987—Exotic 1977 Federal agencies directed to restrict the introduction of exotic species

Organisms (Carter 1977a) into natural ecosystems.

Executive Memorandum on 1994 Prescribed use of regionally native plants for landscaping Federal

Environmentally and Economically grounds, Federal projects, and Federally funded projects using low

Beneficial Practices on Federal input landscaping practices.

Landscaped Grounds (Clinton 1994)

Executive Order 13112— 1999 Directed agencies to provide for restoration of native species and

Invasive Species (Clinton 1999) habitat conditions in ecosystems invaded by exotic species.

a

For text see: Cornell Law School, Legal Information Institute (2000).

revolve around genetic considerations, social acceptance of

site preparation practices such as herbicide use or chaining,

the use of exotics to control weeds or to reduce the spread of

wildfires, protection of threatened and endangered plant

and animal species, and preservation of local gene pools.

Drastically Disturbed Lands

Early efforts to reclaim mine disturbances on public

lands emphasized the use of exotic grasses and forbs to

provide rapid site stabilization and forage for livestock and

wildlife. Sharply increasing public awareness and concern

for environmental issues in the 1960s and the greater

private funding available to meet compliance for bond

release for revegetation of mined lands effected a gradual

shift to the inclusion of greater numbers of native species

in seeding mixes (Redente and Keammerer 1999). The

Surface Environment and Mining Program (SEAM), chartered by the Forest Service in 1973, sponsored technology
50 USDA Forest Service Proceedings RMRS-P-21. 2001

Monsen and Shaw Development and Use of Plant Resources for Western Wildlands

transfer programs and encouraged research that contributed substantially to plant material development, revegetation technology, and further growth of the native seed

and plant industry (for example, see USDA Forest Service

SEAM n.d.; USDA Forest Service 1979). The Surface Mining Control and Reclamation Act of 1977 (SMCRA; P.L. 95-

87; 30 U.S.C. 1201 et seq.) (Cornell Law School, Legal

Information Institute 2000) reinforced these efforts, mandating “a diverse, effective, and permanent vegetative

cover of species native to the disturbed land or species that

will support the planned post-mining uses of the land.”

The SEAM Program and the SMCRA contributed to major

advances in technology and plant materials development for

revegetation of other disturbed lands. Plant materials selected primarily for mined land revegetation by universities

and USDA NRCS Plant Materials Centers, Agricultural

Research Service and Forest Service received widespread

use. Development of seed and seeding technology, revegetation equipment, and plant propagation protocols facilitated

use of an increased number of species. Research related to

plant succession, weed invasions, and competitive interactions in mixed plantings on mined sites increased knowledge

of native flora and led to overall advances in wildland

revegetation.

DePuit and Redente (1988) examined long-term results

obtained from seedings of native and introduced species on

mined lands. They determined that introduced species might

be more appropriate for rapid control of erosion. However,

they found a stronger relationship between mature community structure and composition of the seed mix when native

rather than exotic species were seeded. Although cost and

establishment of native species were problematic, they concluded that reestablishment of native communities offered a

number of advantages compared to exotic seedings. These

included greater sustainability, lower management inputs,

ease of integrating management of reestablished communities and surrounding native communities, and better quality of wildlife habitat produced.

Big Game Ranges

A wide assembly of ecotypes of shrub species considered

important for big game ranges in Utah were collected for

field trials prior to 1970. These plantings, coupled with

seed germination and establishment studies, provided data

required to support the release of a number of widely

adapted woody and herbaceous cultivars by the USDA

Forest Service, Utah Division of Wildlife Resources, and

cooperators (McArthur, this proceedings). Some of these

cultivars and an increasing number of other species were

brought into cultivation for production of seeds for restoring big game ranges while seeds of others continued to be

collected from wildland stands.

Establishment and maintenance of a seed warehouse by

the Utah Division of Wildlife Resources aided in improving

the availability of native and exotic species and ecotypes

(table 2). This agency established procedures for purchasing

a constant supply of seed each year, stabilizing the market

and assuring sufficient sales to promote collection and

marketing a number of species. It defined seed quality

standards, delineated geographical regions or collection

zones, and developed procedures to clean seeds of many

native species. Other agencies and users benefited from this

effort, as more species became increasingly available to a

growing number of buyers. As seeds of additional species,

particularly shrubs, began to be marketed regularly, it

became possible to revegetate more shrub-dominated

communities.

A number of seed companies specializing in the sale of

native plants were established by the mid 1970s and provided a more constant supply of seed, particularly species

required for game habitat improvement. The Utah Division

of Wildlife Resources continued to support seed production

studies for species grown under cultivation. Commercial

growers who used information obtained from these studies

were able to rapidly expand seed production.

Two rather important changes in revegetation priorities

altered the emphasis on species selection for plantings.

Prior to about 1980, considerable emphasis was given to

planting key winter browse species such as antelope bitterbrush, fourwing saltbush, Stansbury cliffrose (Cowania

mexicana D. Don var. stansburiana [Torr.] Welsh), and

mountain mahoganies (Cercocarpus H. B. K. spp.) (Giunta

and others 1978; Stevens and others 1977; Tiedemann and

Johnson 1983; Tiedemann and others 1984). These and

other species were commonly planted on sites where they

did not naturally occur. Attempts to establish and maintain the shrubs in “offsite” growing conditions, particularly

degraded sagebrush rangelands, were eventually recognized as being ecologically unsound. Seeding mixes were

reevaluated to include species that were site adapted regardless of their forage traits. In addition, sagebrush and

rabbitbrush, once the focus of agency weed eradication

programs, gradually gained acceptance as appropriate

revegetation species. This contributed to a major shift in

seed demands (Rosentreter and Jorgensen 1986). Species

of sagebrush and rabbitbrush are now among the most

widely seeded.

Recent declines in stands of some native species and

populations have impacted revegetation priorities. Cheatgrass expansion and increased wildfire frequency have resulted in the loss of extensive stands of antelope bitterbrush,

Stansbury cliffrose, mountain mahogany, and Wyoming big

sagebrush (Artemisia tridentata Nutt. ssp. wyomingensis

Beetle and Young). In many cases the loss of these stands

has severely limited the use of ecotypes that once dominated

large areas.

Table 2—Number of native and introduced species seeded by the Utah

Division of Wildlife Resources during selected years from

1959 to 1999a.

Origin Life form 1959 1969 1979 1989 1999

Native

Grasses 0 4 6 9 19

Forbs 0 6 8 8 9

Shrubs 8 16 22 20 12

Introduced

Grasses 9 9 11 15 11

Forbs 3 4 7 14 8

Shrubs 1 0 1 1 1

a

Walker 2000.
USDA Forest Service Proceedings RMRS-P-21. 2001 51

Development and Use of Plant Resources for Western Wildlands Monsen and Shaw

Wetlands and Riparian Areas

Improvement of degraded riparian systems became a

major management concern in the Western United States

in the late 1970s and early 1980s (Swanson 1988). Damage

to streams and associated riparian areas resulting from

livestock grazing practices and other human activities

impaired watershed function, decreased biological diversity, and adversely impacted economic and recreational

activities both locally and downstream. Growing public

recognition of the magnitude of these problems led to

efforts to improve stream functioning and riparian condition through improved management or, when necessary,

through active restoration (Kauffman and Krueger 1984;

Skovlin 1984; Thomas and others 1979).

Concern over the condition of wetland and riparian areas

also led to formulation of Federal policy to preserve and

restore these habitats. Direction was provided by such

documents as the Clean Water Act of 1972 (P.L. 92-500; 33

U.S.C. 1251 et seq.) (Cornell Law School, Legal Information

Institute 2000) and amendments directing pollution control

of streams, lakes, and estuaries; Executive Order 11988—

Floodplain Management (Carter 1977b); and Executive Order 11990—Protection of Wetlands (Carter 1977c). Additional legislation and programs including the “Swampbuster”

Provisions of the Food Security Act of 1985 (P.L. 99-198; 7

U.S.C. 1281 et seq.) and the Conservation Reserve Program

authorized by this Act, the North American Wetlands Conservation Act of 1989 (P.L. 101-233; 16 U.S.C. 4401 et seq.),

and the Wetlands Reserve Program authorized by the Food,

Agriculture, and Conservation and Trade Act of 1990 (P.L.

101-624; 16 U.S.C. 3801 et seq.) support restoration and

management of degraded wetlands, primarily on private

lands (Cornell Law School, Legal Information Institute

2000; Mitsch and Gosselink 1993; Tzoumis 1998; White and

others 1992). Both the Conservation Reserve Program and

the Wetlands Reserve Program are administered by the

USDA NRCS.

Restoration of disturbed wetland and riparian areas requires that affecting factors first be identified and controlled

at the watershed level to restore proper hydrologic and

biologic functioning. In many cases, adjustments in management permit natural recovery of riparian vegetation in these

systems (Goodwin and others 1997; Hawkins and others

1997; Landers 1997). Seeds or vegetative material may be

planted when active restoration is dictated by loss of seed or

plant sources, drastic declines in the water table, or other

factors. Wetland and riparian plantings have centered on

the use of native species, and where possible, local populations (Borman 1996; Carlson 1992; Hughes 1996; Lambert

1995; Willard and Reed 1986). Vegetation in wetland and

riparian areas exhibits high species diversity. Thus, revegetation of these areas has generated a demand for seed and

planting stock of numerous species receiving little use in the

past, but which are now often included on the availability

lists of many nurseries and seed dealers.

Many wetland species are distributed across wide geographic and elevational ranges. Local accessions are generally selected for planting as little is known about genetic

variation or the range of adaptation of individual populations within these species. Numerous riparian species spread

vegetatively; plugs, wildings, rhizome sections and cuttings

of these species are easily propagated and planted. Container seedlings, larger plants, cuttings, or poles are used on

unstable sites prone to flooding and in areas where the water

table declines substantially in summer. Results of recent

research on seed germination requirements, the relative ease

of storing and handling seeds, and concern for disturbances

created by collection of vegetative material are contributing

to increased use of seed for propagating riparian species.

The USDA NRCS Plant Materials Program has played a

key leadership role in the selection and use of plant materials for riparian and wetland areas. Research conducted by

Plant Material Centers provides much of the available data

on variability within wetland and riparian species (Flessner

and others 1992) as well as guidelines for their propagation

and planting (Hoag 1995). Guides developed by the USDA

NRCS aid in selection of native species that can be used

successfully for revegetation within Major Land Resource

Areas (Lambert 1999) or larger geographic areas (Bentrup

and Hoag 1998; Lambert 1995; Ogle and others 2000). In

addition, the agency has released a series of source-identified wetland and riparian plant materials for use when local

sources of seed or vegetative material are not available

(Englert and others 1999).

Wildfires and Weed Invasions

Throughout the twentieth century, the invasion of cheatgrass (Bromus tectorum L.) and other annual weeds onto

rangelands degraded by excessive livestock grazing and

other disturbances contributed to lengthened fire seasons

and increased fire frequencies (Whisenant 1990; Young and

others 1987). The annual grass/fire cycle enhances the

spread of annual and perennial weeds, destroys native

communities, and reduces ecosystem resilience (Entwistle

and others 2000; McArthur and others 1990; Monsen and

Kitchen 1994). By 1992 about 1.3 million ha of USDI BLM

lands were dominated by annual grasses, and 30.8 million

ha of public rangelands were weed infested or susceptible to

invasion (Pellant and Hall 1994). From 1991 to 2000 an

average of 645,113 ha of USDI BLM lands burned each year

(USDI BLM 2000a). Post-fire rehabilitation efforts to reduce

the spread of weeds, fuel buildup, and ecosystem simplification are conducted on a landscape scale and have provided a

major impetus to growth of the wildland seed industry (table

3). The USDI BLM Emergency Fire Rehabilitation Handbook provides guidance for these projects and prescribes the

use of native materials when available (USDI BLM 1998).

Executive Order 13112—Invasive Species prescribes use of

native materials to restore areas invaded by weeds (Clinton

1999). Introduced species received extensive use in the past

due to their availability, low price, and ability to establish in

low precipitation areas with high potential for weed invasion. Recent developments in site preparation techniques at

the research and application levels offer promise of aiding

the establishment of native species (Meyer and others 2000;

Pellant and others 1999; Shaw and Monsen 2000). The

increasing availability and use of native grass seed cultivars, particularly of native wheatgrasses including thickspike

wheatgrass (Elymus lanceolatus Scribn. & J. G. Smith),

Snake River wheatgrass (Elymus wawaiensis J. Carlson),

and western wheatgrass (Pascopyrum smithii [Rydb.]) as
52 USDA Forest Service Proceedings RMRS-P-21. 2001

Monsen and Shaw Development and Use of Plant Resources for Western Wildlands

well as wildland harvested Wyoming big sagebrush caused

the balance of USDI BLM purchased seed to shift to regionally native species (Pellant and Monsen 1993) (table 3).

However, the need to further diversify seedings in terms of

species and populations and associated challenges are

recognized.

Although many problems remain, efforts to restore native

communities on rangelands over the last 2 decades have led

to major advances in development of equipment for site

preparation and seeding of mixtures and trashy seeds at

appropriate rates and depths. Innovative methods are being

implemented to insure seed availability and origin. Seed

warehousing by the USDI Bureau of Land Management in

Boise, Idaho, has added a measure of stability to the seed

industry, improved the availability of seed supplies, and

provided cold storage facilities for short-lived seeds.

National Forests have traditionally seeded introduced

annual and perennial grass and forb cultivars and available

native grass cultivars to provide soil stabilization following

forest fires. However, concerns exist that the seeded grasses

fail to provide adequate protection during the first season

post-fire, and that the introductions may be highly persistent, sometimes invasive, and preclude recovery of native

vegetation (Clark and McLean 1979; Powell and others

1994; Robichaud and others 2000). A recent update of the

USDA Forest Service Burned Area Emergency Rehabilitation Handbook prescribes use of genetically local sources of

native plants when possible or nonpersistent, noninvasive

species if local material is not available (USDA Forest

Service 2000d). Some National Forests are promoting the

collection of local seed sources and seed increase of selected

grasses and forbs. Seed transfer guidelines for the most

commonly used shrubs are being developed for the Intermountain area (Mahalovich 2001a,b).

The magnitude of the wildfire and weed issues has

contributed to the establishment of government programs

and initiatives for plant materials development and use.

The USDI BLM Green Stripping Program (Pellant 1990)

was established in 1984 to develop technology for establishing fuel barriers to protect existing shrublands and plant

materials for restoring native communities. Executive Order

13112—Invasive Species prescribed restoration of native

species and habitats, where possible, on areas invaded by

alien species (Clinton 1999). The extreme fire seasons of

the last decade (1991 to 2000) contributed to development

of the Great Basin Initiative, a proposal that provides a

blueprint for planning and implementing a restoration

program for Great Basin Ecosystems (USDI BLM 2000b).

Other Land Disturbances

Native and introduced plant materials are used for revegetating or mitigating an array of disturbances on public and

private lands. The USDA NRCS and USDI National Park

Service have collaborated since 1989 on a program to develop plant materials for revegetating roadway disturbances

in National Parks (Haas 2001; Link 1993). To date, plant

materials of more than 800 accessions of native species have

been tested and increased, and 9,000 kg of seed and 520,000

seedlings have been produced through this agreement (Haas

2001). The U.S. Department of Transportation, Federal

Highway Administration, provides policy guidance for revegetation conducted by State Departments of Transportation.

Several Western States have native wildflower programs;

current challenges are to combat invasive weeds and reestablish native species and communities where practical

(Harper-Lore 1999, 2001). The Federal Native Plant Conservation Memorandum of Understanding, originally signed by

10 Federal agencies in 1994, established a committee to

identify conservation needs for native plants, including the

restoration of native species on public lands and promotion

of similar activities on private lands. To date, 174 public and

private organizations have signed on as cooperators with the

committee (Plant Conservation Alliance 2001). This organization has the lead within Department of the Interior agencies to increase the availability of native plants (Office of

Management and Budget 2001).

The Conservation Reserve Program (CRP), managed by

the USDA NRCS, compensates landowners for retiring

highly erodible land for 10 years (USDA Farm Service

Agency 2001a). Providing the seed required for plantings on

these lands has created a challenge for the conservation and

wildland seed industry. From 1987 to 2001 nearly 4.4 million

Table 3—Seeds purchased by the USDI Bureau of Land Management, Denver Federal Center, in three 2001 buysa.

Origin not specified

Certified site-identified BLM specified origin or noncertified, variety

or certified variety or noncertified variety not specified

Origin Life form Species Varieties Pounds Species Pounds Species Pounds

Native

Grasses 16 23 1,448,300 13 246,600 6 52,950

Forbs 0 0 0 2 2,100 4 28,650

Shrubs 5 3 180,710 9 559,060 6 32,945

Total 21 26 1,629,010 24 807,760 16 114,545

Introduced

Grasses 11 15 664,100 7 527,300 1 1,000

Forbs 6 6 290,350 4 133,900 3 24,400

Shrubs 1 1 5,300 1 157,800 0 0

Total 18 22 959,750 12 819,000 4 25,400

aUSDI Bureau of Land Management (2001).
USDA Forest Service Proceedings RMRS-P-21. 2001 53

Development and Use of Plant Resources for Western Wildlands Monsen and Shaw

ha of CRP lands in the 11 Western States were planted with

introduced grasses to improve soil stability, while another

6.9 million ha were planted with regionally native grasses

(USDA Farm Service Agency 2001b). Plantings to improve

wildlife habitat were installed on about 250,000 ha. During

many years, insufficient seed of requested species, cultivars,

or specific populations has been available for both CRP

plantings and post-fire seedings on public lands. The result

is that prices escalate and alternatives to the desired species

mix are often purchased and seeded.

Genetic Considerations in Selecting and

Using Plant Materials

Research during the past quarter century has considerably

increased our knowledge of genetic diversity in western

wildland species (for example, see McArthur, this proceedings). However, much remains to be learned regarding variability within individual species. Seed collectors, seed growers, nurserymen, agency personnel, revegetation practitioners,

and researchers recognize that genetic considerations must

play a role in selecting planting materials for revegetating

disturbances. Controversy has arisen over the use of native

versus exotic species, definitions of “native,” and specifications for selection of native plant materials in order to preserve local populations (Belnap 1995; Gutknecht 1992; Millar

and Libby 1989; Pyke 1996; Rice 1996). At issue is the

question of whether gene flow between the seeded and local

populations of cross-pollinated species will impede natural

selection in the local populations and “swamp” or “pollute”

their gene pool, or whether local populations might be

outcompeted if nonlocal sources are planted, regardless of the

plant’s breeding system (Jones 1997b; Linhart 1995; Millar

and Libby 1989; Rice 1996). At the same time, introgression

can be an important evolutionary force, creating new gene

complexes and potentially greater adaptability (Jones and

Johnson 1998).

Researchers have attempted to provide frameworks for

making appropriate plant material selections. Monsen and

McArthur (1995), for example, proposed classifying sites

into two categories:

Type 1—Sites that are badly degraded or otherwise changed

by loss or change of topsoil or by radical change of topography,

hydrology, or fire cycles, or that have a high priority use such

as watershed protection. These sites should be treated with

the most appropriate plant materials available, indigenous or

non-indigenous, for meeting critical objectives such as site

stabilization, weed control, or protection of watershed values.

Type 2—Sites with good potential for restoration to natural

conditions. These sites should be treated and managed to

return them to near predisturbance conditions.

Jones and Johnson (1998) recommend first assessing the

site potential and desired landscape for the disturbance,

determining seeding objectives, and considering the genetic

integrity of materials to be used. The latter includes selection of material genetically similar to that occurring on the

site and insuring that genetic shifts are minimized throughout the propagation cycle. Practical considerations or feasibility factors then enter into the process. These include seral

status of the disturbance, examination of the presence or

potential for weed invasions, and economic constraints.

Within this framework the species list is reassessed and

finalized. Appropriate genetic material for each species

must then be selected. Scale of the disturbance, time and

economic limitations, and seeding objectives often dictate

the degree to which specific gene pools can be selected. Local

seed sources are much more likely to be available for smallscale plantings than for portions of the sagebrush steppe

heavily impacted by large fires.

Selection of appropriate plant materials is hindered by our

limited knowledge of the reproductive biology and genetics

of individual wildland species. For introduced species, selection generally involves identification of the cultivar most

suited to the planting site. For natives, the problem is more

complex. Ecotypes, biotypes, and chromosome races occur

within many species and may be selected for specific site

conditions (Borman 1996; Jones 1997b; Jones and Johnson

1998). For more extensive disturbances, collections of a

single taxa gathered from sites throughout the area may be

combined to form multiple component plant materials. These

provide broad genetic diversity and adaptation to the range

of conditions encountered within the disturbance (Jones

1997b; Millar and Libby 1989; Munda and Smith 1995; Stutz

1983). Materials released through the variety or pre-varietal release program may be options when local seed sources

are unavailable. Plant breeding techniques may be utilized

to overcome specific problems such as seed dormancy that

prevent the use of a species for revegetation (Jones 1997b).

Plant breeding approaches such as the use of multiple

component materials and modified convergent-divergent

selection processes are used to breed plant materials with

increased rather than narrowed genetic diversity for potential use on extensive disturbances (Munda and Smith 1995).

Seed Certification

Early revegetation plantings generally utilized seed harvested from noncertified stands of introduced or native

grasses or from wildland stands of natives. Selection trials

for improved plant materials suitable for revegetation work,

generally grasses, were conducted using agricultural plant

selection and breeding methods and materials were released

to commercial growers as cultivars through State Crop

Improvement Associations. The International Crop Improvement Association, organized in 1919 with members in the

United States and Canada and renamed the Association of

Official Seed Certifying Agencies in 1968, fostered development of improved crop varieties, uniform naming of cultivars, and a certification system for regulating the propagation, multiplication, and dissemination of improved seed

(Copeland and McDonald 1985). The four generation system

adopted led to production of “blue tag” or certified seed,

which provides growers with assurance of genetic purity and

acceptable quality. Field isolation requirements, checks for

weeds and off-types, and inspection of seed conditioning,

quality, and identity are some of the services provided

through the certification system (Copeland and McDonald

1985). Limitations on numbers and lengths of generations

that cross-pollinated varieties may be grown outside the

area of use are applied when necessary to reduce the risk of

genetic drift.

Some of the earliest cultivars used on wildlands were

released in the 1940s. Examples include the introductions
54 USDA Forest Service Proceedings RMRS-P-21. 2001

Monsen and Shaw Development and Use of Plant Resources for Western Wildlands

‘Manchar’ smooth brome released in 1943 and ‘Greenar’

intermediate wheatgrass released in 1946 (Englert and

others 1999), and the natives ‘Bromar’ mountain brome

(Bromus carinatus H. & A.) and ‘Primar’ slender wheatgrass

(Elymus trachycaulus [Link] Gould ex Shinners) released in

1946. The USDA Natural Resources Conservation Service,

Agricultural Research Service, and Forest Service; land

grant universities; and other public and private entities

continue important programs to test individual species for

range of adaptation and specific desirable traits and to

develop widely adapted releases for wildland seedings

(Alderson and Sharp 1994; Englert and others 1999;

McArthur, this proceedings). Physiological tests including

measurements of respiration and temperature have been

developed in an attempt to provide a more rapid assessment

of adaptability than the normal series of field trials (Jones

and others 1999; McArthur and others 1998; Monaco and

others 1996; Smith and others 1996).

The formal release system generally functions well for

introduced grasses and legumes and for some native species

that can be reliably produced in seed fields or seed orchards.

However, the highly ecotypic nature of many wildland species, low seed production, and problems encountered in

producing some species under agricultural conditions due to

difficulties encountered in harvesting, conditioning, planting, and stand establishment hindered cultivar development for other important native species. Erratic or limited

market conditions and storage problems associated with

some species further frustrated these efforts. Most woody

species require several years of growth before producing

seed, thus slowing testing and establishment of shrub seed

orchards and reducing the opportunity for economically

viable production. In light of these and other problems and

the numerous species, ecotypes, and local populations potentially required for revegetation efforts, seed collectors

and growers have employed a variety of methods in addition

to the formal release process for providing plant materials

for revegetation. Grass and forb seeds are collected from

wildland stands where they can be mechanically harvested

or easily hand harvested. Shrub seeds are collected from

major wildland stands or from areas producing good seed

crops in a given year. Some easily grown, nonselected populations are planted in seed fields or orchards and harvested.

Agencies and other entities purchasing seeds have adapted

approaches for obtaining seeds from desired species and

locations. The Utah Division of Wildlife Resources purchases and warehouses seeds from specified areas to meet

anticipated needs. The USDI Bureau of Land Management

may specify specific stands for collection with agency overview (Fritz 2001). In British Columbia, the Ministry of

Forests has published a general transfer guideline for nontree

species and recommended that the use of the same seed

planning zones developed for trees be applied to these

species (Bakker 1999).

Buyers, however, have continually faced difficulties in

obtaining adequate quantities of seeds of known origin to

insure that the seed source will be adapted to planting

conditions. In an attempt to deal with this problem, The

Association of Official Seed Certification Agencies has developed a Source Identified seed program for revegetation

species by modifying the long-established Source Identified

program utilized for tree seed (Currans and others 1997;

Young 1995, 1996; Young and others 1995). This program

applies to both wildland-collected and field-grown seed or

vegetative material of indigenous or nonindigenous species.

Verification of identity for field-grown seed is conducted as

for the traditional release system. Due to limitations of

personnel and funding, however, onsite inspections of wildland collections often occur for only a fraction of the applications (Currans and others 1997).

The alternative “Source-Identified” or “Pre-variety Germplasm Certification” Program is considered a “fast track”

approach for making available genetically manipulated or

nongenetically manipulated (natural track) plant materials

of known origin when there is an immediate need for the

material, alternative sources are not available, or market

limitations preclude the development of the germplasm to

the cultivar status (AOSCA 1997). Germplasms are designated “Source-Identified” when the geographic origin is

known, but no comparisons have been made with other

germplasms of the species. “Selected Class” germplasm

demonstrates promise of superior or unique traits when

grown in common gardens with other germplasms of the

same species, while “Tested” germplasm maintains these

traits through progeny testing. “Tested” germplasms may be

released as named cultivars if they are found to be widely

adapted and market conditions warrant the release (Young

1995, 1996; Young and others 1995). Most material released

through this program falls into the nongenetically manipulated “Natural” category. Within each category, plant materials are further identified by the number of generations

they are removed from their origin. As with the traditional

certification program, the number of generations permitted for seed production and the restrictions on the number

of years seed may be collected from a perennial seed field or

orchard vary among species (AOSCA 1997). Although not

adopted until 1993, the Pre-variety Germplasm Certification program is seeing widespread use. More than 50

percent of USDA NRCS releases during the 1990s were

released through this program (table 4). In Utah, 95,262 kg

of wildland collected seed were Source-Identified in 1999

(Young 2001). About 23 percent of USDI Bureau of Land

Management native shrub seed purchases based on weight

of pure live seed were Source-Identified in 2000 (table 3)

(USDI BLM 2000c).

Seed Quality

The last 25 years have seen major advances in the development of procedures for testing the seed quality of native

and introduced species used for revegetation. Difficulties

are encountered due to the large number of species, subspecies, and varieties being used and the extreme variability in

morphology, dormancy, and germination requirements encountered among taxa, populations, and years of collection.

Reliable measurements of seed quality are critical for setting and comparing seed prices and for calculating seeding

rates. Numerous studies of the seed ecology and biology of

revegetation species have been conducted over the last

quarter century (see references in McArthur, this proceedings, for contributions of the Shrubland Biology and Restoration Project and cooperators alone). However, resources

expended for the study of even common species are extremely limited compared to research funding for individual
USDA Forest Service Proceedings RMRS-P-21. 2001 55

Development and Use of Plant Resources for Western Wildlands Monsen and Shaw

Table 4—U.S. Department of Agriculture, Natural Resources Conservation Service plant releases by decade, 1950 to 1999a.

1950–1959 1960–1969 1970–1979 1980–1989 1990–1999

Pre-varietal Pre-varietal Pre-varietal Pre-varietal Pre-varietal

Origin Life form releases Cultivars releases Cultivars releases Cultivars releases Cultivars releases Cultivars

Native

Grass 0 5 3 11 0 24 0 27 39 24

Forbs 1 0 2 0 0 7 0 9 21 4

Shrubs 0 0 0 1 0 9 0 24 8 13

Trees 0 0 0 0 0 10967

Introduced

Grasses 10 15 1 13 1 13 0 15 2 10

Forbs 4 3 4 7 1 6 0 10 0 7

Shrubs 0 0 0 1 0 80401

Trees 0 0 0 0 0 40216

a

Englert and others 1999.

agricultural crop species. The seed biology of many native

genera and species remains essentially unknown.

Seed laws in most States require that a licensed laboratory test the seed lots before or at the time of sale (Currans

and others 1997). Problems have occurred throughout the

history of revegetation efforts in the Western United States

because tests were not always completed and seed of very

low quality was sometimes sold. Some laboratories do not

accept seed lots of species for which there are no rules.

Others accept seed lots and apply tests developed in-house

with procedures and results varying from laboratory to

laboratory. The Association of Official Seed Analysts (AOSA)

and other organizations have attempted to address problems associated with testing native seeds. A user’s guide to

the procedures, values, and interpretation of seed tests and

results was developed by the Western Forest and Range

Seed Council in 1986 (Stein and others 1986). In 1998 the

AOSA organized a symposium that addressed problems and

progress in native seed testing (AOSA 2001).

Tests most commonly conducted include purity, seed

weight, and germination or viability. Problems encountered

in purity testing result largely from inadequate or nonrandom sampling. For some species, further problems are introduced by differences in interpretation of the seed unit

(Kitchen 2000). Purity testing is particularly problematic for

species such as winterfat (Ceratoides lanata [Pursh] J. T.

Howell) or prostrate kochia (Kochia prostrata [L.] Schrader)

that typically produce many small or empty fruits and for

sagebrush, rabbitbrush, and other species that are often sold

at low purities. In addition, purity tests for such seed lots can

be extremely time consuming and costly. Recommendations

for sampling and quantities of seed required for testing,

refined definitions of the seed unit for problematic species,

and training sessions for users as well as seed analysts are

included among approaches for improving estimates of purity and their interpretation (AOSA 2000; Currans and

others 1997; Stein and others 1986).

Although the average numbers of seeds per kilogram have

been published for many species (AOSA 2000; Redente and

others 1982; Schopmeyer 1974; Stevens and others 1996;

Vories 1980), these can differ immensely among populations

and collection years. The number of seeds per kilogram is

also dependent upon the extent to which various structures

surrounding the fruit or seed are removed during cleaning

(Kitchen 2000). Thus, in many cases tests of individual seed

lots are necessary for completing seeding rate calculations.

Assessments of seed germinability and viability are critical to determination of seed quality. New AOSA rules for

testing germination of additional wildland species are

being developed, refereed, and adopted each year (AOSA

2000). Cooperative agreements (1985 to 1989 and 1997 to

present) between the Utah Department of Agriculture

(now Utah Department of Agriculture and Food), the Utah

Division of Wildlife Resources, and the Shrub Sciences

Laboratory have contributed to the adoption of 37 rules for

widely used revegetation species (Kitchen 2000; McArthur,

this proceedings). Difficulties arise when species without

rules must be used. Currans and others (1997) reported

that 67 percent of the species sold by two Utah seed

companies, including many commonly sold species with

named cultivars, did not have rules. Additional problems

arise as native and exotic revegetation species often exhibit

extreme dormancy, and variability in dormancy and germination requirements often occur among and within seedlots

of individual taxa. Development of additional rules and

innovative approaches for testing germination of species

exhibiting variability in germination requirements within

or among populations are needed to reduce these problems

(Kitchen 2001).

Viability testing using tetrazolium chloride staining is

often used as an alternative to germination testing when a

rule is not available or when lengthy time periods are

required for germination (Peters 2000). A revised handbook

on tetrazolium testing prepared through collaboration by

the AOSA and the Society of Commercial Seed Technologists

(Peters 2000) updates the original handbook that emphasized agricultural species, primarily grasses (Grabe 1970).

The new volume provides procedures for 103 families and

375 genera. Difficulties continue due to differences in interpretations of embryo staining, inadequate analyst experience and training, and a need for additional guidelines.

Limitations result from the inability of viability tests to
56 USDA Forest Service Proceedings RMRS-P-21. 2001

Monsen and Shaw Development and Use of Plant Resources for Western Wildlands

detect dormancy, minor seed damage, disease, fungal infections, or chemical or fungicide damage (Vankus 1997). Additional research on viability testing and opportunities for

analysts to work with individual wildland species are needed

to further improve the value of viability tests (Currans and

others 1997).

Site Preparation and Planting

Development of effective site preparation and planting

practices and equipment have been major goals of revegetation research in the Intermountain area from the beginning

(Holmgren 1956; Jordan n.d.; Plummer and others 1957).

Reducing competition on rangelands infested with annual

grasses and rapidly spreading perennial weeds (Sheley and

Petroff 1999) and planting mixtures of species with diverse

seeds across extensive and irregular terrain present complex problems. As a greater array of native species are now

being planted together to reestablish more complete communities, seedbed preparation and planting methodologies

must become more complex. Seeds of individual species

require specific seeedbed conditions and emerging seedlings

differ widely in resource requirements and growth rates.

Seeds of different species often must be planted at different

depths and seeded at different rates to attain desired densities. Through the efforts of the Revegetation Technology and

Equipment Committee (originally the Equipment Development Committee, later renamed the Vegetative Rehabilitation and Equipment Workshop), commercial enterprises,

agency personnel, and others, major advances in revegetation equipment development have occurred over the last two

decades. However, modification of agricultural equipment

and the design and fabrication of equipment for the relatively small rangeland market continue to pose a challenge

for commercial enterprises.

Disturbed rangelands generally support competitive weeds

that must be controlled if new plantings are to survive and

establish. Mechanical tillage, burning, and herbicides treatments are frequently employed to reduce competition. A

major challenge has recently arisen in the restoration of

rangelands where retention of residual species is desired.

Remnant native broadleaf herbs, grasses, and shrubs often

persist in low numbers in degraded communities. These

plants may provide critical seed sources ultimately needed

to repopulate the site. Selective treatment to reduce competition and establish desired species is accomplished by

interseeding strips or patches within the area to initiate or

hasten natural recovery. Improved approaches for

interseeding would find widespread application.

Literature and Databases

Numerous efforts have been made over the last 25 years

to summarize research data on the use of native and

introduced species for revegetation and to make it more

readily available to users. The U.S. Department of Agriculture, Agriculture Handbook 450, Seeds of Woody Plants in

the United States, originally published in 1948 and expanded in 1974 (Schopmeyer 1974), summarized data of

use to nurserymen and seed dealers for propagation of trees

and woody shrubs. The book was again revised by Young

and Young (1992), and is currently undergoing a major

revision and expansion by the USDA Forest Service (USDA

Forest Service 2000e). Numerous other publications summarize information on germination of wildland grasses,

forbs, shrubs and trees. Some also include ecological information, propagation techniques, and planting and seeding

recommendations (for example, Bentrup and Hoag 1998;

Carlson and McArthur 1985; Fulbright and others 1982;

Landis and Simonich 1982; Link 1993; McArthur and

others 1978; Monsen and Shaw 1983; Monsen and Stevens,

in review; Redente and others 1982; Rose and others 1998;

Smith and Smith n.d.; Stevens and others 1996; Vories

1980; Wark and others 1995; Wasser 1982; Young and

Young 1986). Similar information is becoming more available on the Internet. Examples include the Plants Database, a source of information on plants of the United States,

including their use as plant materials (USDA NRCS 2000);

Vegspec, a web-based decision support system for planning

revegetation programs (USDA NRCS and others 2000); the

Plant Materials Program, which describes USDA NRCS

Plant Materials and their availability (USDA NRCS 2000);

the Native Plants Network with protocols for propagation

of native plants (University of Idaho 2000); the National

Tree Seed Laboratory (USDA Forest Service 2000b); Grass

Varieties in the United States (Alderson and Sharp 1994);

and the State and Private Forestry Reforestation, Nurseries and Genetic Resources Program with information on

nursery management and propagation of forest and conservation seedlings (USDA Forest Service 2000c). The Native

Plants Journal, first published by the USDA Forest Service

and the University of Idaho in January 2000 (University of

Idaho 2000) features papers on plant propagation and use

of native plants.

Conclusions____________________

Monsen and Christensen’s 1976 paper listed five areas for

future plant materials research emphasis: (1) further study

of the range of adaptability of species and ecotypes being

used; (2) selection and development of additional species and

ecotypes for revegetation uses; (3) development of a dependable supply of high-quality seeds and transplanting stock;

(4) improvements in site preparation and planting procedures for the establishment of shrubs on rangelands; and (5)

reduction of plant losses to insects and diseases. All of these

themes remain important today. The last 25 years have seen

important advances in all phases of revegetation science and

applications. Rather than focusing on specific uses, the aim

of revegetation now is to restore functional plant communities dominated by adapted native species where practical.

Additional work is needed to provide the research data and

verification procedures to ensure selection of adapted seed

sources and maintain their identity. To accomplish true

restorations, there is a need to develop revegetation technology for additional species. Seed production guides are generally provided with cultivar releases, but seed production and

propagation techniques are needed to provide adequate seed

and plant supplies of numerous other species (Jones 1997a;

McArthur and Young 1999). Germination and viability procedures must be developed for more species, and new approaches taken to reduce inconsistencies in laboratory test

results (Kitchen 2001). Adequate storage facilities are needed
USDA Forest Service Proceedings RMRS-P-21. 2001 57

Development and Use of Plant Resources for Western Wildlands Monsen and Shaw

to permit accumulation of seeds in good production years,

improve availability of commonly used species and sources,

and stabilize the seed industry. Additional site preparation

and seeding technology and equipment are required to

provide weed control and permit seeding of diverse seed

mixtures. Understanding of establishment requirements

and species interactions is needed to successfully reestablish diverse plant communities.

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William T. Sommers is Director, Vegetation and Management Protection

Research Staff, USDA Forest Service, PO Box 96090, Washington, DC

20090-6090.

Scientific Challenges in Shrubland

Ecosystems

William T. Sommers

Abstract—A primary goal in land management is to sustain the

health, diversity, and productivity of the country’s rangelands and

shrublands for future generations. This type of sustainable management is to assure the availability and appropriate use of scientific information for decisionmaking. Some of most challenging

scientific problems of shrubland ecosystem management are nonnative invasive species, probable effects of global climate change,

detrimental effects due to land use change, restoration of degraded

environments, and maintaining the quality and quantity of water.

Introduction ____________________

One of the primary goals of land managers and landowners in the Western United States is to sustain the health,

diversity, and productivity of our Nation’s rangelands and

shrublands to meet the needs of present and future generations. Effectively meeting this goal requires current information about the land and its resources, an understanding

of the public’s wishes, and actions that support the environment, the economy, and the local community. Key to attaining this goal is the availability of scientific information and

the appropriate use of that information in informing

decisionmaking. Sustainable management provides research

the context and purpose to address some of our most difficult

scientific challenges in shrubland ecosystems. These challenges include the: (1) biological invasion by nonnative

invasive species, (2) probable effects of global climate change,

(3) detrimental effects due to land use change, (4) restoration

of degraded environments, and (5) maintaining the quality

and quantity of water.

Nonnative Invasive Species _______

These species are one of the greatest threats to rangeland

health, even though they might be considered both a cause

and consequence of ecosystem degradation. Invasive species

can compromise an ecosystem’s ability to maintain its structure or function and can dramatically increase fire frequency and intensity, reduce property values, and increase

management costs. In the future, it is likely that these

impacts will be exacerbated by global climate change because scenarios suggest more favorable conditions for the

introduction and spread of invasive species.

Scientific information is critically needed to prevent and

mitigate the extensive invasive species damage on our

rangelands. It is crucial that more emphasis be placed on

pathway analyses, risk assessments, and predictive models.

Further research and development is also needed on the

biology and ecology of invasive species, their host-site relationships, and monitoring protocols.

Probable Effects of Global Climate

Change ________________________

Our current natural ecosystems are threatened by the

probable effects of global climate change. Future scenarios

suggest that the rate of global climate change will increase

and the magnitude and frequency of ecological processes will

likely be greater in the next 100 years. This means there may

be many scientific uncertainties. Science and technology

opportunities need to focus on reducing the risks of climate

change and adapting to the inevitable changes. Additional

efforts are needed in assessing potential thresholds and

breakpoints, improving long-term data sets and baseline

indicators to measure environmental conditions, assessing

the impacts of multiple stresses, and focusing on future

changes in severe weather and extreme events.

Detrimental Effects Due to Land Use

Changes _______________________

Shrublands play a key role in sequestration and greenhouse gas emissions. However, their location, composition,

and health are noticeably changing because of land use

changes. These land use changes have the potential to alter

the balance between emissions and absorption and negatively impact ecological conditions. We need to understand

the physical, biological, and social interactions within a

fragmented landscape. Land use change research should

include remote sensing, modeling techniques, and spatial

analysis products to improve this understanding.

Many of our Nation’s watersheds are deteriorating at

alarming rates. Degraded, poorly functioning ecosystems

limit our management options and increase the expense and

frequency of our management activities. This degradation

and disturbance can include a loss of ecosystem resilience

and productivity, accelerated erosion and impaired soil

development; accumulations of nutrients and chemicals,

alterations in the biogeochemical cycles and hydrologic

pathways, artificial and simplified structure and composition, modification of interactions and dynamics, reductions

in biological diversity; and deterioration of water quality.
USDA Forest Service Proceedings RMRS-P-21. 2001 63

Scientific Challenges in Shrubland Ecosystems Sommers

Restoration of Degraded

Environments __________________

Whether the cause is an influx of invasive species or

harmful environmental effects due to land use change, there

are an increasing number of acres needing restoration, an

increasing number of conflicts over treatment options, and

rising restoration costs. These trends indicate that lagging

ecological restoration represents a major impediment to

sustainable management of ecosystems at individual sites

and at landscape scales. Clearly, there is a major need for

additional investments in restoration science. Additional

efforts are needed to study economic costs, benefits, risks,

and efficacy of restoration options, prioritization methods

for restoration actions, postrestoration prediction models,

and performance monitoring. Areas for restoration emphasis should include ecosystems impacted by nonnative invasive species, degraded high-priority watersheds, and fire

damaged lands.

The urgency of the restoration challenge facing resource

managers and users is increasing. The demands of expanding human populations and development are making it

progressively more difficult to conserve native flora and

fauna, and to sustain the delivery of ecosystem goods and

services from increasingly degraded public lands and waters. Degraded, poorly functioning ecosystems significantly

limit management options. Nevertheless, public land and

resource management agencies are mandated to protect and

restore the health and productivity of the ecosystems entrusted to their stewardship. Unfortunately, management

policies and practices are inadequate and in some cases

inappropriate for restoring ecosystems to fully functioning

condition. This management inadequacy is largely because

the scientific basis for restoration based on understanding of

the structure, composition, and function of ecosystems and

their resilience to human and natural disturbance is

inadequate.

Maintaining the Quality and

Quantity of Water _______________

Healthy watersheds play a vital role in maintaining the

integrity of our water systems to supply people with drinking water, recreation, and commodities. Reducing erosion

and contaminated runoff, maintaining soil quality and productivity, and safeguarding water quality and quantity will

help maintain healthy watersheds. Research focusing on

stream corridors and riparian areas, abandoned minelands,

and headwaters is needed to perpetuate healthy watersheds. Basic and applied research on the effects of land

management on the functioning of watershed and riparian

landscape features and long-term process studies on fire and

grazing continue to be of important in providing a scientific

basis for restoring sensitive watersheds.

Our research can provide insight into long-term trends in

the health and productivity and provide critical data to

identify or predict potential changes caused by these scientific challenges.

In closing I would like to stress the importance of accountability. We need to do a better job documenting the impact

of these scientific challenges and highlighting the value of

the shrubland resource. This documentation requires consistent, comprehensive information. The Montreal Process

Criteria and Indicator framework (figure 1) is an operational

framework that provides reliable and accurate resource

condition information about the extent, condition, and trend

of sustainability across the landscape. This common language can communicate to a wide array of audiences across

multiple scales, climatic zones, regions, agencies, and ownership boundaries while the consistent methodology provides a foundation for effectiveness and warning of critical

issues. The Montreal Process, as it pertains to rangelands,

is described in a special issue (volume 7 number 2) of “The

International Journal of Sustainable Development and World

Ecology” (Flather and Sieg 2000; Joyce 2000; Joyce and

others 2000; McArthur and others 2000; Mitchell and Joyce

2000; Neary and others 2000).

Thank you for the invitation to give this presentation. I

look forward to hearing more about the exiting new knowledge and technologies that are developing to help us sustain

the health, productivity, and diversity of our private and

public shrublands.

Criterion #2

Productivity

Capacity

Criterion #1

Biological

Diversity

Criterion #3

Ecosystem

Health

Criterion #4

Soil/Water

Conservation

Criterion #5

Global Carbon

Cycles

Criterion #6

Socio-Economic

Benefits

Criterion #7

Legal, Institutional,

and Economic

THE

MONTREAL

PROCESS

Figure 1—Seven criteria (shown here) and 67

criteria make up the Montreal Process.
64 USDA Forest Service Proceedings RMRS-P-21. 2001

Sommers Scientific Challenges in Shrubland Ecosystems

References _____________________

Flather, C. H.; Sieg, C. H. 2000. Applicability of Montreal Process

Criterion 1—conservation of biological diversity—to rangeland

sustainability. International Journal of Sustainable Development and World Ecology. 7: 81–96.

Joyce, L. A. 2000. Applicability of Montreal Process Criterion 5—

maintenance of rangeland contribution to global carbon cycles.

International Journal of Sustainable Development and World

Ecology. 7: 138–149.

Joyce, L. A.; Mitchell, J. E.; Loftin, S. R. 2000. Applicability of

Montreal Process Criterion 3—maintenance of ecosystem

health—to rangeland sustainability. International Journal of

Sustainable Development and World Ecology. 7: 107–127.

McArthur, E. D.; Kitchen, S. G.; Uresk, D. W.; Mitchell, J. E. 2000.

Applicability of Montreal Process Criterion 2—productive capacity—to rangeland sustainability. International Journal of Sustainable Development and World Ecology. 7: 97–106.

Mitchell, J. E.; Joyce, L. A. 2000. Applicability of Montreal Process

biological and abiotic indicators to rangeland sustainability:

introduction. International Journal of Sustainable Development

and World Ecology. 7: 77–80.

Neary, D. G.; Clary, W. P.; Brown, T. W., Jr. 2000. Applicability of

Montreal Process Criterion 4—soil and water conservation—to

rangeland sustainability. International Journal of Sustainable

Development and World Ecology. 7: 128–137.
USDA Forest Service Proceedings RMRS-P-21. 2001 3

Genetics and

Biodiversity

65

USDA Forest Service Proceedings RMRS-P-21. 2001 67

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Joan Vallès is Professor, Laboratori de Botànica, Facultat de Farmàcia,

Universitat de Barcelona, Av. Joan XXIII, s/n, 08028 Barcelona, Catalonia,

Spain. E. Durant McArthur is research geneticist and project leader, Shrub

Sciences Laboratory, Rocky Mountain Research Station, Forest Service,

United States Department of Agriculture, Provo, Utah 84606, USA.

Artemisia Systematics and Phylogeny:

Cytogenetic and Molecular Insights

Joan Vallès

E. Durant McArthur

Abstract—The genus Artemisia (Asteraceae, Anthemideae, Artemisiinae) is a large genus, one of the largest genera in its family. It

is comprised of about 500 taxa at the specific or subspecific level,

distributed in 5 sections or subgenera. Most species are perennial

and many are landscape dominants of arid or semiarid regions.

Artemisia is widely distributed in the Northern Hemisphere but

poorly represented in the Southern Hemisphere. It is more richly

represented in Eurasia than it is in North America. A number of

Artemisia species have a high economic value for food, medicine,

forage, ornamentals, and other uses. Some taxa are invasive weeds,

which can adversely affect harvests. Even though some features

(carpological and palynological ones) are quite constant and characteristic of the genus, a high degree of morphological variation exists.

Artemisia has two basic chromosome numbers, with ploidy levels

ranging from diploid to dodecaploid for x = 9 and from diploid to

hexaploid for x = 8. Polyploidy and dysploidy are two very relevant

evolutionary mechanisms in the genus, particularly the first one,

which is present in all its major groups. The classical systematics of

Artemisia have been refined by molecular methods, for example,

internal transcribed spacer (ITS) sequences of nuclear ribosomal

DNA, chloroplast DNA restriction site (cpDNA) data, and randomly

amplified polymorphic DNA (RAPD) analysis but in the main hold

well. This presentation provides a general introduction and characterization of Artemisia with particular emphasis on its systematics

and evolution as illuminated by cytogenetic and molecular data.

Introduction ____________________

Artemisia, one of the larger genera in the family Asteraceae

and the largest genus in the tribe Anthemideae, comprises

from 200 to more than 500 taxa at the specific or subspecific

level (depending on the authors, for example, Bremer and

Humphries 1993; Ling 1991a,b, 1995a,b; Mabberley 1990;

McArthur 1979), which are distributed in 5 sections or

subgenera (Torrell and others 1999b). Many Artemisia species have a high economic value in several fields. Some

examples are as food plants (absinth–A. absinthium–and

other taxa, such as A. genipi, used in preparation of liquors);

as spices (tarragon or estragon–A. dracunculus); in medicine, as an antihelminthic (A. santonicum and related taxa)

and a new promising source of anti-malaria biochemicals

(A. annua); as forage (A. herba-alba and related species in

African and Asian steppes and semideserts and A. tridentata

and its allies in North American shrublands); as ornamentals (A. absinthium, A. caucasica, and A. stelleriana among

many others); and as soil stabilizing agents in badly disturbed habitats, for example, highways, railroads, and mines

(A. ludoviciana and A. vulgaris)—see Bailey Hortorium

Staff (1976) and Turner and Wassen (1999) for general

reference. On the other hand, some taxa, such as A. verlotiorum, are invasive weeds, which can adversely affect

harvests. Some others may be toxic (A. absinthium, for

instance) or causative of pollen-induced allergies (the Iberian endemic A. barrelieri among others; Giner and others

1999). Marco and Barberá (1990) give a conspectus of the

chemical composition of Artemisia, and revisions of applied

aspects of the genus can be found in Pareto (1985) and Tan

and others (1998). The high number of taxa, the dominance

of some of them in landscapes, and the usefulness of many of

them have attracted the interest of the researchers, who

have produced a considerable amount of literature concerning Artemisia in many disparate fields of study (systematics

in all its approaches, ecology, chemistry, pharmacology, and

so forth). This paper provides a general review of different

systematic and evolutionary aspects of the genus, with

special emphasis on cytogenetic and molecular data.

Life Form and Morphology ________

Artemisia species are most commonly shrubs, rarely perennial herbs and more rarely annual or biennial herbs.

Thus, perennial plants largely dominate the genus; only 5

percent of the taxa (approximately 10 species) are annual or

biennial species. Leaves are alternate or sparse, usually

more or less divided (exceptionally entire, such as in A.

dracunculus and A. cana), with extremely variable shapes

and dimensions. Flower heads are small, basically ovoid,

cylindrical or hemispheric in shape, constituted by a rather

small number (4–40) of flosculose florets (lacking ligulate

ones), and grouped in racemose or paniculate synflorescences.

Fruits are pappus-lacking achenes or cypselas, characteristic of the genus (Korobkov 1981; Ouyahya and Viano 1985,

1990; Persson 1974; Vallès and Seoane 1992). Palynological

characters are useful markers for the genus Artemisia. The

weak (verrucose) exine ornamentation contrasts with the

higher (spinulose) one of the other members of the tribe

Anthemideae, as already pointed out by Wodehouse (1926)

and confirmed by later authors (Dimon 1971; Vallès and

others 1987). Some of the morphological traits of Artemisia

(non-opposite leaves, absence of radial florets, non-paleate

head receptacle, many capitula with few florets in each
68 USDA Forest Service Proceedings RMRS-P-21. 2001

Vallès and McArthur Artemisia Systematics and Phylogeny: Cytogenetic and Molecular Insights

synflorescence, achenes without pappus) are considered

phylogenetically derived characters, within the phylogenetically advanced family Asteraceae (Cronquist 1977).

Phenology and Reproductive

Biology ________________________

Phenology is a good distinctive trait for Artemisia in

respect to the remaining Anthemideae or Asteraceae genera. Most Artemisia species flower in autumn; however, a

few taxa start flowering in summer and others flower in the

winter. In the Northern Hemisphere, the flowering period

ranges from June to January and fruiting period from

August to March. Pollination is basically anemogamous;

Artemisia and closely related genera are the only tribe

Anthemideae genera that have this kind of pollination

(Heywood and Humphries 1977; Leppick 1970), evidently

related to the pollen ornamentation; nevertheless, frequent

insect visits have been reported in different species of the

genus, which makes it reasonable to think that a certain

percentage of entomogamous pollination occurs (GarnockJones 1986; Vallès 1989). Even though they lack the pappus

(except for the distinctive A. papposa), the achenes of Artemisia are at least partly anemochorous due to their very

small dimensions and low weight. Zoochory and hydrochory

also have significance in the genus. Artemisia shows a

relatively low capability of fruit dispersion far from mother

plants and a relatively high seedling mortality index. These

dispersal disadvantages are compensated for and plants are

efficiently propagated due to high fruit productivity, germination rates, and general plant vigor (Bostock and Benton

1979; Oliva and others 1997; Vallès 1989; Walton and others

1986).

Ecology and Geographical

Distribution ____________________

Artemisia species are found in many ecosystems: from

desert communities (A. santolina in Uzbekistanian and

Iranian deserts, for instance) to humid environments

(A. molinieri, an endemic species to southeastern France

and A. cana ssp. bolanderi, endemic to the Oregon area of

the United States, the only taxa in the genus to live in

temporarily inundated soils); from near sea level (A.

caerulescens from European marine salt marshes) to the top

of high mountains, at almost 4,000 m (the Iranian A.

melanolepis and the North American A. pattersonii and A.

scopulorum); some species are ruderal (as A. vulgaris). The

genus is widely distributed in the Northern Hemisphere but

uncommon in the Southern Hemisphere (only about 10

species). Most Artemisia species grow sparsely or form small

populations, but several taxa form large, expansive populations and characterize landscapes. Different steppe and

semidesert shrubby communities are dominated by species

belonging to the subgenera Seriphidium (Mediterranean

region, Central Asia) or Tridentatae (North America).

Classification ___________________

In such a large genus, it is to be expected that many

attempts have been made to establish an infrageneric

classification. The main proposals are compared in Table 1,

where we can see that some large infrageneric groups are

more or less present in all Artemisia classifications. Besser

(1829, 1832, 1834, 1835) and Candolle (1837) established

these groups as sections. They follow and are based on a few

morphological characters:

Artemisia (originally named Abrotanum Besser). Heterogamous capitula with outer florets female and central

florets hermaphrodite, and fertile and glabrous receptacle.

Absinthium DC. Heterogamous capitula with outer

florets female and central florets hermaphrodite and

fertile and hairy receptacle. Some authors merge this

section into the precedent one.

Dracunculus Besser. Heterogamous capitula with

outer florets female and central florets hermaphrodite

but female-sterile and glabrous receptacle. Cassini

(1817) transferred the species of this section to a new

genus, Oligosporus Cass.

Seriphidium Besser. Homogamous capitula with all

florets hermaphrodite and fertile and glabrous receptacle.

Table 1—Comparison among different infrageneric classifications of Artemisia.

Category Infrageneric taxa Reference

Genera Absinthium Abrotanum Artemisia Tournefort (1700)

Genus Artemisia Linné (1735)

Genera Artemisia Oligosporus Cassini (1817); Lessing (1832)

Sections Absinthium Abrotanum Seriphidium Dracunculus Besser (1829, 1832, 1834, 1835);

De Candolle (1837)

Subgenera Euartemisia Seriphidium Euartemisia Rouy (1903)

Subgenera Absinthium Abrotanum Seriphidium Dracunculus Rydberg (1916)

Sections Seriphidium Tridentatae

Subgenera Artemisia Seriphidium Dracunculus Polyakov (1961b)

Subgenera Absinthium Artemisia Seriphidium Dracunculus Persson (1974)

Sections Artemisia Dracunculus Tutin and others (1976)

Subgenera Artemisia Seriphidium Tridentatae Dracunculus McArthur and others (1981)

Subgenera Artemisia Seriphidium Dracunculus Podlech (1986)

Genera Artemisia Seriphidium Artemisia Ling (1991a,b)

Subgenera Artemisia Seriphidium Dracunculus
USDA Forest Service Proceedings RMRS-P-21. 2001 69

Artemisia Systematics and Phylogeny: Cytogenetic and Molecular Insights Vallès and McArthur

Rydberg (1916) created the new section Tridentatae Rydb.

to include the main part of North American Seriphidium,

which he treated as a subgenus. McArthur (McArthur and

others 1981) elevated this section to the subgeneric level.

Ling (1982, 1991a,b, 1995a,b) proposed separation of one of

the main Artemisia sections (or subgenera) as a large (almost 150 species) independent genus, Seriphidium (Besser

ex Hook.) Fourr. (table 1). Bremer and Humphries (1993)

and Bremer (1994) have accepted this segregation in their

cladistic revisions of the tribe Anthemideae and the family

Asteraceae, respectively.

Some small (even monotypic) genera have also been removed from Artemisia, such as FilifoliumKitam., Kaschgaria

Poljakov, NeopallasiaPoljakov, TuraniphytumPoljakov, Elachanthemum Y. Ling & Y.R. Ling, Artemisiella A. Ghafoor,

ArtemisiastrumRydb., MausoleaPoljakov and Picrothamnus

Nutt. (Bremer and Humphries 1993; Ghafoor 1992; Ling

and Ling 1978; Poljakov 1961a; Rydberg 1916). However,

many current treatments retain these proposed segregates

within Artemisia. Most of the genera included in the subtribe

Artemisiinae contain some species previously described as

members of Artemisia.

Cytogenetics ___________________

Artemisia chromosomes are rather small (2–8 μm). Karyotypes tend to be symmetric, considering both the interchromosomal and the intrachromosomal asymmetry (McArthur

and Plummer 1978; McArthur and Pope 1979; McArthur

and others 1981; Mendelak and Schweizer 1986; Oliva and

Vallès 1994; Schweizer and Ehrendorfer 1983; Vallès and

Siljak-Yakovlev 1997); they fit into 2A and 2B classes

(Stebbins 1971). The use of Giemsa C-banding and chromomycin and bisbenzimide fluorochrome banding (Mendelak

and Schweizer 1986; Oliva and Vallès 1994; Schweizer and

Ehrendorfer 1983; Vallès and Siljak-Yakovlev 1997; Torrell

and Vallès, unpublished data on file at Laboratori de Botànica,

Facultat de Farmàcia, Universitat de Barcelona) provide

the opportunity to use heterochromatic chromosome segments banding patterns—called banding style by Schweizer

and Ehrendorfer (1983)—for systematic study. There is a

predominance of telomeric bands over intercalary and centromeric bands. Chromomycin-positive (GC-rich) bands appear often linked to the nucleolus organizing regions in

satellited chromosomes. Preliminary studies using fluorescent in situ hybridization (FISH) show that 18S rDNA tends

to be located in the chromomycin-positive regions (Torrell

and others, unpublished data on file at Laboratori de

Botànica, Facultat de Farmàcia, Universitat de Barcelona).

The general pattern basically characterized by telomeric

bands is also found in other genera of the tribe Anthemideae

(Schweizer and Ehrendorfer 1983). B chromosomes have

been reported in different numbers (1–5) in some species and

populations of the genus (McArthur and others 1981;

McArthur and Sanderson 1999a; Torrell and others 1999a,

2000; Vallès and Siljak-Yakovlev 1997; Torrell and Vallès,

unpublished data on file at Laboratori de Botànica, Facultat

de Farmàcia, Universitat de Barcelona).

The genus has two basic chromosome numbers, the largely

predominating x = 9 and the less extended x = 8. X = 9 is not

only the most common basic number in the genus Artemisia,

but in the tribe Anthemideae and the family Asteraceae as

well (McArthur and Sanderson 1999; Oliva and Vallès 1994;

Schweizer and Ehrendorfer 1983; Solbrig 1977; Vallès and

Siljak-Yakovlev 1997). A single species has been reported at

x = 7 (Artemisia pattersonii—Wiens and Richter 1966). We

do not believe this isolated circumstance warrants consideration as a basic chromosome number for the genus; rather,

we believe this must have been an aneuploid reduction. Two

phenomena have been basic in the chromosome evolution in

the genus: polyploidy and dysploidy.

Polyploidy

Apart from being a common evolutionary mechanism in

plants, it has been widely recognized as particularly active

in Artemisia (Ehrendorfer 1964, 1980; Estes 1969; Koul

1965; McArthur and Pope 1979; McArthur and others 1981;

McArthur and Sanderson 1999; Oliva and Vallès 1994;

Persson 1974; Torrell and others 1999b, 2000; Vallès 1987a,

1987b; Vallès and Siljak-Yakovlev 1997). A high percentage

of Artemisia species are polyploid. This phenomenon is

present in all the major groups into which the genus is

divided. Both basic chromosome numbers show polyploidy,

with levels up to 12x for x = 9 and 6x for x = 8. The

circumboreal, but largely Eurasian, Artemisia dracunculus,

for which the chromosome numbers 2n = 18, 36, 54, 72 and

90 have been reported (Kawatani and Ohno 1964; Rousi

1969) constitutes a good example of a complete series from

diploid to decaploid levels, based on x = 9. The large, western

North American subgenus Tridentatae (= sagebrush), also

based on x = 9, provides another robust example of polyploidy from diploid (2n = 18) to octoploid (2n = 72) levels

(McArthur and Sanderson 1999). The dodecaploid level has

been reported to now only for one species, A. macrantha

(Malakhova 1990). For x = 8, the Artemisia vulgaris group

shows a series from diploid to hexaploid levels (Vallès 1987a;

Vallès and Torrell, unpublished data on file at Laboratori de

Botànica, Facultat de Farmàcia, Universitat de Barcelona).

Recent studies (Torrell and Vallès 2001) show that nuclear

DNA content (ranging approximately from 3 to 27 pg) is well

correlated with ploidy level, and that evolutionary trends in

genome size in the genus comprise both decreases and

increases in DNA content, as it has been reported to happen

in other groups belonging to the family Asteraceae (Cerbah

and others 1999; Price and Bachmann 1975).

Dysploidy

The existence of two basic numbers shows Artemisia as a

dysploid genus. Dysploidy is present in three of the main

groups in the genus (Artemisia, Absinthium and Dracunculus); Seriphidium and Tridentatae display only one basic

number, x = 9. Kawatani and Ohno (1964) inferred that

x = 9 was the original basic number from the fact that it is

the most common one in the genus. Vallès and SiljakYakovlev (1997) found evidence for a chromosomal fusion in

A. vulgaris, which experimentally supported the hypothesis

that descending dysploidy in the genus is derived. This 2n =

16 species has a chromosome pair much longer than the

remaining 7 pairs. This long pair of chromosomes is almost

perfectly metacentric and includes a centromeric
70 USDA Forest Service Proceedings RMRS-P-21. 2001

Vallès and McArthur Artemisia Systematics and Phylogeny: Cytogenetic and Molecular Insights

heterochromatic region. In addition to that, this chromosome pair shows a high centromeric fragility, so that both

arms of every chromosome often appear distinctly separated

after squashing. These traits are evidence of a chromosomal

fusion. This can explain the appearance of a number of x =

8 based species, as well as the existence of some erroneous x

= 9 based counts for some of these taxa. Subsequent research

has confirmed the same fusion syndrome in other species,

such as A. judaica, A. lucentica, and A. reptans (Torrell and

Vallès, unpublished data on file at Laboratori de Botànica,

Facultat de Farmàcia, Universitat de Barcelona), and

A. incana and A. splendens (Torrell and others 2000), representing different groups in which dysploid processes have

occurred. Polyploid x = 8 taxa (for example, A. splendens,

2n = 32) have two larger metacentric chromosome pairs,

confirming the likelihood of a fusion event prior to

polyploidization (Torrell and others 2000). The idea of descending dysploidy as an evolutionary trend is consistent

with what is known in different genera in the family

Asteraceae (Siljak-Yakovlev 1996; Solbrig 1977). Other examples of dysploid processes are known in the tribe

Anthemideae (Heywood and Humphries 1977), even though

this is not a common mechanism in the tribe (Mitsuoka and

Ehrendorfer 1972; Schweizer and Ehrendorfer 1983).

Chromosome Number Evolution

Figure 1 presents a scheme of the putative chromosome

number evolution in Artemisia. The examples described

above illustrate almost all changes in chromosome number

and ploidy level. There is only one point left: the appearance

of 2n = 34 populations or taxa. This chromosome number

may be reached from 2n = 18 through 2n = 36 or from 2n =

16 through 2n = 32. In the first case we cite the example of

A. umbelliformis, with one 2n = 18 subspecies (ssp. eriantha)

and another one (ssp. umbelliformis) for which 2n = 36 and

2n = 34 have been reported (Oliva and Vallès 1994). Chromosome morphology suggests an allotetraploid origin for A.

umbelliformis ssp. umbelliformis, with ssp. eriantha as one

of the ancestors (Ehrendorfer 1980; Gutermann 1979; Oliva

and Vallès 1994); 2n = 34 populations seem stabilized

enough to discard a simple case of aneuploidy and to consider

a dysploid-polyploid origin of a new secondary basic number,

x = 17. Some populations of the A. vulgaris complex may also

have reached this number from 2n = 16 by means of polyploidy and duplication of one chromosome pair (Vallès and

Torrell, unpublished data on file at Laboratori de Botànica,

Facultat de Farmàcia, Universitat de Barcelona).

Molecular Biology _______________

Working on Artemisia it is easy to be convinced that, as

Persson (1974) stated, the currently accepted main groups

within the genus do not represent natural groups. So, different attempts have been made in recent years to refine or

redefine the systematics of the genus to the light of molecular data (Kornkven and others 1998, 1999; McArthur and

others 1998a,b; Torrell and others 1999b). Two main questions (generic delimitation and infrageneric classification)

concerning classification may be addressed by molecular

studies.

Generic Delimitation

As stated above (see Classification section), different authors proposed to segregate some of the main infrageneric

groups in Artemisia, namely Oligosporus (Cassini 1817) and

Seriphidium (Bremer 1994; Bremer and Humphries 1993;

Ling, 1982, 1991a,b, 1995a,b), as independent genera. Phylogeny based on the nuclear ribosomal DNA internal transcribed spacers (ITS-1 and ITS-2) sequences does not support these segregations and shows a monophyletic genus in

its broad, classical sense (Torrell and others 1999b). Molecular data support morphological ones. Only minor morphological-physiological traits (receptacle indumentum and sex

of peripheral florets) separate Dracunculus (the basis for the

genus Oligosporus) and Seriphidium from other main groups

in the genus, whereas major characters, such as pollen and

cypsela morphology, clearly define them as members of the

genus Artemisia.

Infrageneric Classification

ITS sequencing data define five major clades within

Artemisia, which are similar, but not identical, to the five

main groups discussed in the Classification section (above)

(table 1). Figure 2 shows these clades, which have the

following links with the classically recognized groups:

Tridentatae and Dracunculus are delimited as traditionally conceived. Absinthium and Seriphidium are

resolved in clades with the addition of some species up

to now included in Artemisia, a completely fragmented

group in the ITS phylogeny (which agrees with the

extraordinary morphological variation within the

group).

Finally, a clade is constituted by the taxa of the group

of A. vulgaris, the type species of the genus.

The analysis of molecular data shows the monophyly of

subgenus Tridentatae (RAPD: McArthur and others 1998a;

Figure 1—Chromosome

number evolution in the

genus Artemisia.
USDA Forest Service Proceedings RMRS-P-21. 2001 71

Artemisia Systematics and Phylogeny: Cytogenetic and Molecular Insights Vallès and McArthur

Figure 2—Cladogram showing the hypothetical ITS phylogeny of Artemisia (adapted from

Torrell and others, 1999b). Consistency index excluding uninformative characters (CI) = 0.471;

retention index (RI) = 0.740. Numbers above branches are bootstrap percentages and

parsimony jackknife results: first, Lidén and others (1997) bootstrap method; second, Plunkett

and others (1996) bootstrap method; third, parsimony jackknife values. Numbers below

branches are decay indices. ART = Section/Subgenus Artemisia, SER = Section/Subgenus

Seriphidium, ABS = Section/Subgenus Absinthium, DRA = Section/Subgenus Dracunculus,

TRI = Section/Subgenus Tridentatae, OUTG = Outgroup.
72 USDA Forest Service Proceedings RMRS-P-21. 2001

Vallès and McArthur Artemisia Systematics and Phylogeny: Cytogenetic and Molecular Insights

ITS sequencing: Kornkven and others 1998; Torrell and

others 1999b; chloroplast DNA: Kornkven and others 1999)

and clearly supports the independence of this North American endemic group from Seriphidium (Torrell and others

1999b). Bremer and Humphries (1993) and Ling (1995b)

included the members of Tridentatae in the genus Seriphidium, even though different authors had suggested, on

the basis of morphological, karyological or chemical characters, the independence and the convergent evolution of both

subgenera or even a closer relationship between Tridentatae

and Artemisia than between Tridentatae and Seriphidium

(Jeffrey 1995; McArthur 1979; McArthur and others 1981,

1998a,b; McArthur and Plummer 1978; Seaman 1982;Shultz

1986).

Perspectives in the Study of

Artemisia ______________________

The present article has summarized a significant part of

the considerable amount of research carried out in different

fields about the genus Artemisia. We can conclude that it is

a rather well-studied genus, but some of its systematic and

phylogenetic aspects remain unsolved as, for example, the

placement of A. filifolia, A. palmeri, and A. californica, see

Hall and Clements (1923) and McArthur and Sanderson

(1999), or the infrageneric classification (Torrell and others

1999b). Apart from research about applied aspects that are

very relevant in this genus, even though they are not the

main object of this paper, many biosystematic studies—in

morphology, population biology, cytogenetics, and molecular biology, among others—are suitable in order to obtain a

better knowledge of the genus. We believe that karyological

(from chromosome counts to molecular cytogenetics) and

molecular (combining different techniques in as many taxa

as possible) studies in Artemisia and the subtribe to which

it belongs (Artemisiinae) will be effective tools in better

systematic definition.

These further studies may support or contradict the present

evidences and nuances. They may demonstrate that a new

revision of the genus is necessary or contrariwise they may

confirm our present understanding in regard to both the

infrageneric classification and the relationships between

Artemisia and its closely related genera (subtribe Artemisiinae). However, we believe that it is certain that multidisciplinary systematic and phylogenetic studies will

continue on this interesting and important group of plants.

Acknowledgments ______________

We thank Montserrat Torrell (Barcelona) for critically

reading the first version of this paper. The research by JV

that permitted a part of the present review has been subsidized by the following institutions: Generalitat de Catalunya

(Catalan autonomous government: AR83-210, 1983–1984;

1998BEAI400180, 1999), Universitat de Barcelona (AIUB,

1985–1986), and Spanish government (DGICYT: PB-88-

0033, 1989–1991; PB-93-0032, 1994–1996; PB-97-1134;

1999–2001). Research by EDM that lead to this review has

been facilitated by a USDA CSREES grant (91-98300-6157)

and by Pittman-Robertson Agreement W-82-R (Rocky Mountain Research Station and Utah Division of Wildlife Resources, cooperating).

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ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

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Stewart C. Sanderson, USDA Forest Service, Shrub Sciences Laboratory,

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Brigham Young University, Provo, UT.

Abstract—Atriplex canescens (Pursh.) Nutt. is the most widespread species of perennial Atriplex in North America, distributed

from southern San Luis Potosi, Mexico, to southern Alberta and

Saskatchewan, Canada, and from the Pacific Coast of California

and Baja California to Texas, Oklahoma, Nebraska, Kansas, and

the Dakotas. Throughout its distributional range, A. canescens

shows considerable between-population variation. Some of this

variation may be due to phenotypic plasticity, but most of it appears

to be genetic. Mutations, polyploidy, introgressive hybridization,

and segregation from interspecific hybrids all appear to have contributed to its extensive heritable variation. Polyploidy is unusually

common with numerous chromosome races (2x, 4x, 6x, 8x, 10x, 12x,

14x, 20x).

Proper identification is important to the utilization of fourwing

saltbush in reclamation. While many of the races have been named

as varieties, others have not. Even though differentiated by ploidy,

chemical constituents, geographic distribution, and morphological

characters, they may lack sufficient diagnostic differences to allow

facile identification, at least in the herbarium. Rather than combining unnamed races under those that do have a taxonomic name, it

seems better at present not to use the formal infraspecific categories

in treating the fourwing saltbushes, but to consider them all as

races. One new variety, Atriplex canescens var. obtusifolia var.

nov., is described, and the combination Atriplex canescens var.

prosopidium (I. M. Johnston) comb. nov. is made.

Introduction ____________________

Atriplex canescens forms a polyploid complex based on x =

9, with chromosome numbers of 2x, 4x, 6x, 8x, 10x, 12x, 14x,

and 20x (Sanderson and Stutz 1994; Stutz and Sanderson

1979). The most widespread and economically important of

these are the 4x (tetraploid) and 6x (hexaploid), while

diploids and higher polyploids are less widespread or local

endemics.

Atriplex belongs to the order Caryophyllales, in which

many of the taxa differ from other dicots in having perisperm

as a nutritive tissue, rather than endosperm. It seems likely

that lack of endosperm (Cronquist 1988; Cronquist and

Thorne 1994), and therefore of endosperm-based barriers

Chromosome Races of Fourwing Saltbush

(Atriplex canescens), Chenopodiaceae

Stewart C. Sanderson

Howard C. Stutz

against polyploidization (Ramsey and Schemske 1998), may

be a factor in the abundance of polyploidy within these taxa

(Sanderson and others 1999). Another somewhat distinguishing factor of Atriplex may be the ability for multisomic

segregation in polyploids with little meiotic irregularity,

probably both for genic reasons (Jackson and Casey 1979) as

well as small chromosome size (Ruas and others 1998;

Stebbins 1971). An apparent intolerance of taxa in the

Chenopodiaceae to aneuploidy is worth noting. Practically

the entire family has a base number of x = 9 (exceptions are

Spinacia and Camphorosma, x = 12, and a few species with

x = 8 and 7 in Chenopodium) (McArthur and Sanderson

1984), and it can also be inferred that the frequency of

chromosomal reorganization is low. Because of these and

possibly other characteristics, the cytogenetic behavior of

chenopods is somewhat different than that of dicots in

general. Examination of meiotic behavior in numerous species hybrids in Atriplex suggests that little chromosomal

differentiation exists between North American perennial

species (Stutz and Sanderson, unpublished data on file at

Brigham Young University). As a result, hybrids tend to be

fertile and meiotic behavior in polyploids is, therefore, probably of an autoploid type, even when hybridization between

species is involved.

This paper presents a key and descriptions for fourwing

saltbush chromosomal races, along with commentary upon

their nature and possible origins.

Methods and Materials ___________

Chromosome counts were made by acetocarmine squash

methods (Sanderson and Stutz 1994). More than 1,800

individuals from 800 populations were counted over a number of years. Flavonoids were identified as aglycones by

paper chromatography using aluminum chloride as a color

reagent (Sanderson and Stutz 1994), and more than 1,200

determinations for fourwing saltbush taxa were made

(table 1). Populations were examined in the field, and

representative specimens deposited at BRY and other

herbaria.

Results and Discussion __________

Establishment of Polyploidy

Because of different probabilities of cytological events at

successive ploidy levels, distinct pathways of polyploidization

appear to predominate at the diploid, tetraploid, and hexaploid levels in North American Atriplex. At the diploid level,
76 USDA Forest Service Proceedings RMRS-P-21. 2001

Sanderson and Stutz Chromosome Races of Fourwing Saltbush (Atriplex canescens), Chenopodiaceae

an interesting type of chromosome number increase seems

to prevail, which we term polyploidization by introgression.

When it happens that a diploid population comes into sympatry with a tetraploid, possibly genetically dissimilar or

even a separate species, unidirectional introgression from

the diploid into the tetraploid may result (Lowe and Abbott

2000; Petit and others 1999; Qu and others 1998; Stebbins

1971; Zohary and Nur 1959). If this occurs, and providing

that the diploid enjoys sufficient numerical dominance, the

tetraploid may be significantly altered by the introgression,

Table 1—Discriminative flavonoid characters of fourwing saltbush. All taxa also produce the

common flavonols kaempferol, quercetin, and isorhamnetin (not listed). Besides the

universally present unsubstituted flavonols, derivatives modified at the 3 or 6 positions

may be observed, as shown below, and tricin, a flavone, is also present in certain taxa.

Number of 6-methoxy- 3-0-methylsamples substituted substituted

examined flavonols flavonols Tricin

2x

Angustifolia (Mexico) 15 – + –

Angustifolia (USA) 60 – – –

Brevis 48 – + –

Garrettii 21 – + –

Gigantea 31 – – –

Linearis 61 +/–(very weak) – +

Piochensis 12 – – –

Stewartii 2 – – –

4x

Angustifolia–4x 24 + – –

Aptera 42 + – –

Bonnevillensis 44 + – –

Canescens 17 + – –

Cunescens 6 + – –

Mexicana 8 – + –

Navajoensis 41 +/–(polymorphic) – –

Occidentalis 330 + – –

6x

Diegensis 10 + – –

Nana 65 +/–(polymorphic) – +

Nevadensis 119 – – +

Occidentalis–6x 28 + – –

Prostrata 9 – + –

Rachelensis–6x 17 + – –

Tooelensis 6 + – –

Vallis 69 + – –

8x

Cuyamaensis (Laciniata–8x) 9 – – +

Obtusifolia 24 + – –

Prosopidium–8x 2 – – +

Rachelensis 11 + – –

10x

Prosopidium 5 – – +

12x

Laciniata 51 – – +

Macilenta 28 – – +

14x

Laciniata–14x 24 – – +

20x

Grandidentatum 33 –a – +

a

Traces are occasionally seen, apparently due to hybridization with Atriplex polycarpa.

eventually to the point that its original racial or taxonomic

identity may no longer be obvious. At that point, if the

population were examined, it would of necessity be categorized as belonging to the race or species of the diploid,

although having a tetraploid chromosomal level.

Unidirectional introgression may be the result of either of

the two more probable cytological mechanisms in this situation, the formation of triploid hybrids, followed by fertilization of their unreduced 3x gametes with x gametes (x + 2x =

3x, 3x + x = 4x), or more directly, the combination of
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Chromosome Races of Fourwing Saltbush (Atriplex canescens), Chenopodiaceae Sanderson and Stutz

introgression from tetraploids into hexaploids. Such introgression seems to be much less widespread, however. While

hybridization appears a factor in formation and development of Atriplex hexaploids, it does not reach the level of

importance inferred for the origin of tetraploidy.

At higher ploidy levels, there are an increasing number of

possible pathways involving unreduced gametes, hybridization, or backcrossing for producing even-ploid offspring at

various ploidy levels. However, these tend to conflict with

each other to prevent easy resolution. The chromosome

number progressions that are observed in the two higher

polyploid series in Atriplex canescens, from the Chihuahuan

and the Sonoran Deserts (Sanderson and Stutz 1994; this

paper), seem to suggest chance isolation of relatively rare

products.

Identification of the Races

Our studies (Sanderson and Stutz 1994; Stutz and

Sanderson 1979, this paper) and those of Dunford (1984,

1985) show that the chromosomal races of Atriplex canescens

are usually identifiable on morphological grounds, as well as

by cytological and geographical criteria. The most generally

useful characters in distinguishing fourwing saltbush races

are the leaf dimensions, notwithstanding the tremendous

seasonal variations exhibited by leaves. Seasonal variation

exists because larger leaves are produced during times of

vigorous growth, while clustered smaller leaves appear in

leaf axils during slower growth on unelongated or partially

elongated shoots. As explained in an earlier report (Sanderson

and Stutz 1994), in seasons of aridity, first the larger and

then successively smaller leaves are shed to reduce water

loss. Some races also produce distinctive winter leaves that

are small, involute, and curled against the stem. As has been

noted in previous studies (Dunford 1985; Sanderson and

Stutz 1994; Stutz and Sanderson 1979), with the exception

of race Garrettii (Garrettii and Stewartii may be considered

separate species from A. canescens proper—see below for

racial description and discussion), diploids have leaf lengthto-width ratios generally above 10:1. This ratio decreases

from diploid to tetraploid chromosome levels, and also somewhat more from tetraploid to hexaploid levels. Foliage color

is generally more yellowish in diploids, apparently because

of reabsorption of a portion of the chlorophyll during arid,

relatively dormant seasons (Munné-Bosch and Alegre

2000), a response that is absent or less noticeable in polyploids. While leaves of all Atriplex species have a covering of

bladder hairs, the Diegensis (6x) race is greener and less

pubescent, while the Rachelensis (8x) race is more graycanescent than most species. Prosopidium (8x, 10x),

Grandidentatum, and others have very abundant hairs,

giving the foliage a whitish or bluish appearance.

Races sometimes also differ in chemical constituents, for

instance, in presence or absence of 6-methoxylated flavonols, as already mentioned. While fourwing saltbushes as

a group produce abundant, bitter triterpene saponins, these

are usually reduced in quantity in races Vallis and Diegensis.

The key to races in this report is somewhat a work in

progress, and it seems likely that with further observation,

characteristics will be identified (for example, winter leaves,

or anther size) that can strengthen racial descriptions.

unreduced gametes from the diploid with normal gametes

from the tetraploid (2x + 2x = 4x) (Lowe and Abbott 2000;

Zohary and Nur 1959). However, since observed introgression between diploids and tetraploids seems exclusively

unidirectional (Stutz and Sanderson, unpublished data on

file at Brigham Young University), a third pathway involving generation of progeny out of the segregation of euploid

gametes in triploids, which might result in bi-directional

introgression, does not appear common.

The relative frequencies of polyploidization by unidirectional introgression versus that for within-population autoploidy, besides depending on ease of hybridization, would

in addition depend on the relative opportunities for establishment of the polyploidized products from each pathway

(both mechanisms are dependent upon the formation of

unreduced gametes). Establishment of within-population

autoploidy would require a relatively unlikely isolation of

the tetraploid products, which could otherwise be swamped

by pollen flow from the diploid parent, leading to sterile

products. In contrast, an established population already

exists by definition for tetraploids in the introgressive

pathway, once introgression has begun, enabling the

polyploidization process to proceed smoothly and rapidly

and to succeed more frequently. Also, as a practical matter,

diploids are weak competitors and easily limited to special

habitats or isolated locations (Sanderson and Stutz, unpublished data on file at Brigham Young University; this paper),

with tetraploids expanding and eventually taking over.

Because of adaptive characteristics that appear to commonly be passed from older tetraploids to the newly formed

ones, fertility and vigor of tetraploid introgressants tend to

be high. One trace of the founding original tetraploid’s

genetic influence that seems to persist in introgressed populations is the enzymatic capacity for flavonol 6-oxygenation,

a trait that is generally absent from diploid perennials

(Sanderson and Stutz 1984) but present in most tetraploid

North American Atriplex. Because of this distribution, flavonol 6-oxygenation is often a useful marker in documenting

the introgressive process.

From the tetraploid level, further polyploidization differs

somewhat from polyploidization out of the diploid level.

Because numerical combinations with unreduced gametes

produced by tetraploids do not readily yield a match for

gametes produced by hexaploids (2x + 3x = 5x; 4x + 3x = 7x;

2x + 6x = 8x; 4x + 6x = 10x), hybridization between tetraploid

and hexaploid populations would not serve directly as a

route for unidirectional introgression. However, an evenploid product can be formed directly from unreduced gametes in tetraploids (2x + 4x = 6x, as opposed to x + 2x = 3x

in diploids) to yield hexaploid offspring. Unreduced gametes

can be inferred to be relatively common at the tetraploid and

higher ploidy levels (Stutz and Sanderson, unpublished data

on file at Brigham Young University). The probability of

spontaneous within-population polyploidization to a higher

level, observed to be rare at the diploid level, might, therefore, be expected to be higher within tetraploid populations.

In fact, hexaploid individuals are observed occasionally in

populations of tetraploid Atriplex canescens (Stutz and

Sanderson, unpublished data on file at Brigham Young

University). These individuals might either become isolated to begin a hexaploid population, or could hybridize

with existing hexaploid taxa to bring about, indirectly,
78 USDA Forest Service Proceedings RMRS-P-21. 2001

Sanderson and Stutz Chromosome Races of Fourwing Saltbush (Atriplex canescens), Chenopodiaceae

Use of Racial and Taxonomic

Designations

As sometimes suggested by molecular phylogenetic studies (Bolger and Simpson 1995; Hardig and others 2000;

Setoguchi and others 1998), and as seen in the evolutionary

behavior of island taxa (Ganders and others 2000; Soltis and

others 1996), speciation may frequently proceed in bursts,

yielding groups of taxa with approximately equal relationships to a common ancestor. Where this type of situation

exists, it would be phylogenetically misleading to lump

arbitrary subsets of the related taxa. Burst-type of speciation has been suggested for North American Atriplex (Stutz

1978) generally, and may be suggested in the present study

by the surprising number of fourwing saltbush races in

lower ploidy levels. Because in fourwing saltbush many of

the races recognized here have not been designated as

varieties or subspecies, it would seem inappropriate to apply

the existing infraspecific categories because the taxonomically unnamed races would then have to be combined with

some of the named taxa. This situation requires that all of

the evolutionary units of fourwing saltbush be granted

taxonomic status, or that formal infraspecific categories be

ignored in favor of racial designations, which is what we

have chosen to do here. It is our opinion, however, that for

utilitarian reasons every evolutionary unit that can be

proven to exist ought to be able to have a taxonomic name,

although it might not then be desirable to include all infraspecific taxa in a flora designed, for example, for field use.

This is an issue that will eventually be dealt with by the

plant taxonomic community, as the number of known instances of cryptic speciation is multiplied and as more and

more plants are studied in detail. Like some other taxonomic

problems, it appears to arise because of fundamental differences in speciation and evolutionary behavior between

plants and animals (Cronquist 1988; Grant 1971), especially

regarding their propensities for hybridization and polyploidization, and the resulting hazard for systematists of

applying inappropriate zoological constructs to plants.

Description of Fourwing Saltbush

Races _________________________

Fourwing saltbush races are listed alphabetically within

ploidy levels, and their taxonomic designations, if any, are

listed.

Race Angustifolia (2x)

Taxonomic nomenclature: Atriplex canescens var.

angustifolia (Torrey) S. Watson, Proceedings of the American Academy of Arts, Sciences and Letters 9: 121. 1874.

Type: Valley of the Rio Grande from El Paso to 40 miles

below San Elceario, Wright 1742 (lectotype NY).

Robust shrub 1–3 m in height, leaves narrowly linear, well

developed leaves during drier parts of the summer only 1–2

(3) mm wide in most populations, flat or slightly folded.

Some growing season leaves usually retained during winter,

often with dwarf, down-curved leaves present on short

shoots. Fruiting wings usually large, 1–2 cm in width, 6-

methoxy flavonols absent.

Angustifolia occurs in New Mexico, westernmost Texas,

some localities in Arizona, and in the Mexican States of

Chihuahua, Coahuila, and southern Nuevo Leon, often on

sand. During warm arid periods, the foliage becomes somewhat yellowish-green, in contrast to the relatively graygreen foliage of Occidentalis (4x) and most other polyploids

of A. canescens. Mexican plants differ from those in the

United States by the production (abundant) of flavonol 3-

methyl ethers (table 1). A form of Angustifolia with more

robust summer and winter leaves occurs in the vicinity of

San Ysidro and Zia Pueblo in New Mexico, and possibly

elsewhere.

In spite of an earlier start of anthesis and only partial

flowering overlap with Occidentalis, Angustifolia gives rise

to numerous intermediate populations at the tetraploid

level that may be called “Angustifolia-4x” (see racial description below). These probably arise through production by

diploid plants of unreduced gametes that unite with the 2x

gametes of tetraploids (2x + 2x = 4x), resulting in rapid oneway introgression, believed to be a common phenomenon in

Atriplex (see above in Results and Discussion). Although

affected tetraploids more or less resemble Angustifolia,

conversion of flavonoid pattern has not been observed, the

synthetic ability for 6-methoxy flavonols being consistently

retained. Leaf length-width ratio and other characters are

seldom also precisely those of diploids. Most tetraploids are

strongly competitive, and have probably replaced diploids

over wide areas.

Race Brevis (2x)

Taxonomic name: none.

Small shrubs to about 0.5 (1) m, growing season leaves

small, narrowly linear. Early growing season leaves reaching about 5 mm in width, dry season leaves only 1–2 (3) mm

in width. Winter foliage of small, folded, down-curved leaves

on short shoots, more or less appressed against the stem, the

summer foliage leaves being shed (sometimes even in the

greenhouse). Fruit including wings usually less than 1 cm in

width, 6-methoxy flavonols absent.

Race Brevis is endemic to the west side of the Rio Grande

Gorge, in northern Taos County, New Mexico, and southernmost Conejos County, Colorado, on basaltic substrates. It

looks like a miniature Angustifolia, short in stature, with

small leaves and relatively small fruits. It is distinguished

at most seasons from Occidentalis and from introgressed

tetraploids in the same area by somewhat narrower leaves

and a more yellowish foliage color. Foliage color has been

observed to be especially useful at a time in the spring when

4x introgressants are actively growing, but Brevis is still in

dormancy. Both of them flower at approximately the same

time.

Like Angustifolia, Brevis appears to cause modification of

adjacent tetraploid populations by one-way introgression,

and numerous dwarf tetraploids are found in northern Taos

County and in San Luis Valley, Colorado. More study is

needed on individual and seasonal variation occurring in

zones of introgression to better distinguish tetraploid

variations from diploids at all times of year.

Brevis differs markedly from Angustifolia in climatic tolerance. San Luis Valley, the habitat of Brevis, is altitudinally
USDA Forest Service Proceedings RMRS-P-21. 2001 79

Chromosome Races of Fourwing Saltbush (Atriplex canescens), Chenopodiaceae Sanderson and Stutz

high, about 2,100 to 2,400 m (7,000–8,000 ft) and, therefore,

exceptionally cold in the winter. Brevis has distinctive

winter foliage, while Angustifolia usually does not seem to,

although more years of observation are needed. Angustifolia

is sufficiently cold sensitive that plants from several sources

all winter killed at Provo, Utah, at an elevation of less than

1,500 m (5,000 ft).

Race Garrettii (2x)

Taxonomic names: Atriplex garrettii Rydberg, Bulletin of

the Torrey Botany Club 39: 312. 1912. Atriplex canescens

ssp. garrettii (Rydb.) Hall & Clements, Carnegie Institute of

Washington, Publ. 326: 344. 1923. Atriplex canescens var.

garrettii (Rydb.) Benson, American Journal of Botany 30:

326. 1943.

Type: USA, Utah, Grand County: vicinity of Moab, Rydberg

& Garrett 8465 (holotype NY, isotypes US, UT, photograph

POM).

Small bushes, usually about 0.3 m or less in height, leaves

oval to obovate, fruiting wings well developed, 6-methoxy

flavonols absent.

Race Garrettii is found on slopes on saline shale and mixed

sandstone-shale, stratigraphically below the Navajo Sandstone, in canyons of the Colorado River drainage in southeastern Utah. After the spring growing season, the foliage

normally becomes a rather bright yellowish-green. Garrettii

is closely related to the tetraploid race Navajoensis (A.

garrettii var. navajoensis), of similar foliage color, but taller

and with longer and slightly narrower leaves, evidently a

derivative of hybridization and one-way introgression involving races Garrettii (2x) and Occidentalis (4x).

Race Gigantea (2x)

Taxonomic name: Atriplex canescens var. gigantea Welsh

& Stutz, Great Basin Naturalist 44: 189. 1984.

Type: Utah, Juab County: Lynndyl sand dunes T35S

R4W, Welsh & Moore 5126 (holotype BRY).

Large bushes, length-width ratio of summer leaves greater

than 10:1, leaf width occasionally reaching 1 cm. Some

smaller leaves of the summer foliage retained in winter

(although more observation is needed), with small shortshoot leaves of winter morphology also present. Fruits large,

to about 2 cm in width including wings, 6-methoxy flavonols

absent.

Endemic to the Little Sahara Dunes, Juab County, Utah.

Tetraploid plants of race Occidentalis grow on shallower,

more stabilized sand at this location, with plants of Gigantea

occurring only on the active dunes (Stutz and others 1975).

The yellowish-green cast often seen in diploids is weaker but

still slightly visible, outside of the spring season of active

growth. Little or no hybridization occurs between Gigantea

and Occidentalis because of a disjunction in flowering time,

Gigantea flowering much later than sympatric Occidentalis.

Race Linearis (2x)

Taxonomic names: Atriplex linearis S. Watson, Proceedings of the American Academy of Arts, Sciences and Letters

24: 72. 1889. Atriplex canescens ssp. linearis (S. Watson)

Hall & Clements, Carnegie Institute of Washington, publ.

326: 344. 1923. Atriplex canescens var. linearis (S. Watson)

Munz, Manual of Southern California Botany 141: 598.

1935.

Type: Mexico, Sonora: in alkaline soil about Guaymas,

Palmer 235 (lectotype GH).

Bushes low except in unusually favorable sites, commonly

about 0.3 m in height, foliage slightly bluish compared to

other Atriplex (fruits and foliage sometimes blackish in

dried specimens), leaves linear, mostly 3 (7) mm wide or less.

Fruiting wings deeply toothed or lobed, very small and

reduced to wing-ridges, or larger and irregular. Fruit body

sometimes hardened and swollen. Fruits, including wings

usually 5–7 (10) mm wide or less, mostly sessile but varying

within a plant from sessile to short pedicellate, or rarely long

pedicellate. Fruiting beaks more or less prominent (the end

of the paired fruiting bracts that extend beyond the winged

part of the fruit), entire, or occasionally 3-toothed, 6-methoxy

flavonols weak or absent.

Plants of this race grow in alkaline or low-lying areas of

the Sonoran Desert of California, Baja California, Arizona,

and Sonora. Linearis bears a strong superficial resemblance

to the 12x race Macilenta (they are combined in Brown

1956), but can be distinguished by foliage color, and the

short or absent fruiting pedicels, and relatively prominent

beak of Linearis. The sometimes spongiform fruit body may

suggest a phylogenetic connection of Linearis to Atriplex

acanthocarpa of the Chihuahuan Desert.

Race Piochensis (2x)

Taxonomic name: none.

Moderate sized shrub, 1 to 1.5 m high, and as in Race

Angustifolia, leaves during the drier growing season narrowly linear. Leaves of winter foliage on short shoots, small,

often folded, but mostly not reflexed, 6-methoxy flavonols

absent.

Piochensis occurs in southern Lake Valley in eastern

Lincoln County, Nevada, at elevations of 1,500 m (5,000 ft)

or greater, with Wyoming big sagebrush or pinyon-juniper.

It shows little of the yellowish color often seen in diploids.

Introgressed tetraploids are widely distributed in the same

area.

Tetraploids with very long and narrow leaves are found at

Overton and Valley of Fire State Park, Clark County, Nevada, 195 km to the south, and may be evidence of a wider

distribution for Piochensis in the past. In addition, a small

population of diploids fairly similar to Piochensis in leaf

color and winter foliage have been found on a sandy reclamation site near Tuba City, northern Arizona (Glenn and

others 1998). Although the seed sources (which included A.

canescens) for the reclamation are unknown, morphological

variation suggestive of fairly widespread introgression into

Occidentalis in the area indicates that the Piochensis-like

plants are native and not just a recent introduction.

Tetraploid populations or individuals having longer and

narrower leaves are also occasionally encountered in northwestern New Mexico. However, Angustifolia occurs along

roadsides in that region, and so either it or Piochensis could

be responsible. In any case, it seems possible there are other

populations of Piochensis not discovered yet. Their location
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Sanderson and Stutz Chromosome Races of Fourwing Saltbush (Atriplex canescens), Chenopodiaceae

might be revealed by the occurrence of Piochensis-like variation among plants of Occidentalis in the locality.

Race Stewartii (2x)

Taxonomic names: Atriplex stewartii I.M. Johnston, Journal of the Arnold Arboretum 22: 110. 1940. Atriplex

acanthocarpa ssp. stewartii (I.M. Johnston ) Henrickson,

Southwestern Naturalist 33: 457. 1988.

Type: Coahuila, Llano de Guaje: margin of playa at base

of Lomas del Aparejo, abundant, erect globose bush 10–16

in. tall, August 28, 1940, Johnston & Muller 777 (holotype

GH).

Suffrutescent plant, leaves narrowly linear to oblong, margins of larger leaves often broadly and shallowly toothed and

wavy. Fruit four-winged, wings well developed, 6-methoxy

flavonols absent.

Stewartii occurs in el Bolson de Mapimí (Mapimi Basin) in

western Coahuila, Mexico. Vegetatively this plant resembles

Atriplex acanthocarpa, but the four-winged fruits suggest

relationship to A. canescens. Winged fruits might have come

about either by hybridization of A. acanthocarpa and A.

canescens, giving rise to Stewartii as a hybrid derivative, or

alternatively, four wings may have been a plesiomorphic

character within ancestors of a group consisting of A.

canescens and most of the North American suffrutescent

species, for example A. acanthocarpa, A. gardneri, and A.

falcata. Observation of breakdown of the four-winged character in A. canescens hybrids suggests that the winged

character is multigenic, with individual loci producing wing

fragments or tubercles by themselves. Tubercles on fruiting

bracts are common in all of the suffrutescent members of this

group, although they are unusually elongated and spine-like

when present in A. acanthocarpa.

Race Angustifolia-4x (4x)

Taxonomic names: none.

Plants more or less resembling Angustifolia (2x), at least

at some times of year, but also somewhat intermediate

between that and Occidentalis (4x), 6-methoxy flavonols

present.

Angustifolia-4x is common in New Mexico, apparently

because of active or previously occurring 2x–4x hybridization. Plants referable to this race are also found in the

Sonoran Desert and occasionally in northern Arizona and

southern Nevada, suggesting a wider distribution of

Angustifolia (2x) or the closely related Piochensis (2x) in

former times. However, they seem to be rare or absent in

Mexican portions of the Chihuahuan Desert, apparently the

ancestral home for Angustifolia (2x).

Race Aptera (4x)

Taxonomic names: Atriplex aptera Nelson, Botanical Gazette 34:356. 1902. Atriplex canescens ssp. aptera (Nelson)

Hall & Clements, Carnegie Inst. of Washington, publication

326: 343, pl. 58. 1923. Atriplex canescens var. aptera(Nelson)

C. L. Hitchcock, Vascular Plants of the Pacific Northwest 2:

186. 1964.

Type: Wyoming: Laramie, September, 1901, Elias Nelson

738 (holotype PH).

Plants mostly low growing, leaves shorter and wider than

in races Occidentalis or Canescens. Fruits usually small, 5–

7 (10) mm in width, fruiting wings lacerate or lobed, wings

often irregular in the sense that some of the wings may be

only partial, and that wing fragments may sometimes grow

between normal wing positions, 6-methoxy flavonols present.

Aptera occurs in Alberta, Saskatchewan, Montana, the

Dakotas, eastern Wyoming, and northwestern Nebraska of

the western Great Plains. The frequently irregular wings of

Aptera are similar to those seen in the hybrids of wingless

species with fourwing saltbush, both as observed in nature

and as produced synthetically. Aptera is believed to have the

parentage of race Occidentalis x Atriplex gardneri. There is

a more or less clinal variation from robust in the south to

slender in the north in Aptera that seems to reflect a series

of separate origins or hybridizations, involving in the south

A. gardneri var. gardneri, and in the north (mostly Canada)

A. nuttallii in the sense of Bassett and others (1983). The

latter might best also be considered a variety of A. gardneri.

Race Bonnevillensis (4x)

Taxonomic names: Atriplex bonnevillensis C. A. Hanson,

Studies in Systematic Botany 1:1. 1962. Atriplex canescens

var. bonnevillensis (C. A. Hanson) Welsh, Great Basin Naturalist 44: 190. 1984.

Type: Utah: Millard County, Desert Range Experiment

Station, dry lake bed 1.5 miles northeast of headquarters,

Hanson 356 (holotype BRY, isotypes K, GH, POM, UC, US).

Plants low growing, fruiting wings lobed or laciniate, often

irregular. Fruits small, usually about 5–7 mm or less in

width, highly variable within and between plants, occasionally wingless, then often resembling those of Atriplex tridentata, with the paired fruiting bracts having three or more

teeth, 6-methoxy flavonols present.

Bonnevillensis is found in a few isolated locations in the

eastern Great Basin desert. The known populations are in

bottomlands or near populations of Atriplex tridentata. It is

of evident hybrid origin, by race Occidentalis crossing with

a suffrutescent species. Hanson (1962), the descriptor, suggested A. falcata (2x except for one known 4x population in

central Nevada), a relatively uncommon taxon of valley

bottoms and slopes with fruiting bracts fusiform and

untoothed, but usually tuberculate, as the second parent.

However, as is the case with some other diploid suffrutescent

species that rarely hybridize, natural hybrids involving

diploid A. falcata are seldom observed. A species more often

hybridizing, and more acceptable on the basis of bract

dentition, is A. tridentata (mostly 6x), a bottomland species

with bracts having side teeth or at least “shoulders.” Origin

from the latter would most likely have required the difficult

derivation of tetraploid individuals by segregation of euploid

gametes (2x) from 5-ploid hybrids (2x + 3x = 5x), while

euploid gametes (3x) appropriate for derivation of hexaploid

individuals should be equally frequent, as confirmed by

Stutz and others (1979). Furthermore, since the presence of

occasional hexaploid individuals in tetraploid Occidentalis,

as commonly observed, should allow facile introgression at

the hexaploid level, a hexaploid overall outcome should be
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Chromosome Races of Fourwing Saltbush (Atriplex canescens), Chenopodiaceae Sanderson and Stutz

strongly favored for hybridization and introgression between race Occidentalis and A. tridentata. The tetraploid

chromosome number of Bonnevillensis is, therefore, surprising. Perhaps, however, the circumstance of an overwhelming preponderance of plants of Occidentalis compared to

those of A. tridentata would be sufficient to tip the balance

towards tetraploidy in spite of these factors. A possible

scenario is as follows: given a small population of A. tridentata (6x) receiving intense pollen rain of race Occidentalis

(4x), much of the reproductive capacity of the hexaploids

would be taken up with production of sterile pentaploid

hybrids, so that they would seldom reproduce. The pentaploids would produce occasional 2x and 3x euploid gametes,

and so, under the pollen rain from tetraploids, their relatively rare offspring would be mostly tetraploid and pentaploid (2x + 2x = 4x; 3x + 2x = 5x). After the original hexaploid

plants had reached the end of their lifespans, only pentaploid and tetraploid plants would remain. The newly formed

tetraploid offspring should reproduce more abundantly, in

comparison with the meager reproductive ability of the

mostly sterile pentaploids. When the pentaploids in turn

had dwindled and died out, the population would then

consist entirely of introgressants at the tetraploid level.

These would continue to receive genetic influence from the

Occidentalis pollen rain as long as the population of

Occidentalis continued to exist nearby, which continues to

be the case at most of the Bonnevillensis sites. Another much

simpler alternative for the origin of Bonnevillensis could

have been by hybridization of Occidentalis with the less

common tetraploid race of A. tridentata.

Race Canescens (4x)

Taxonomic names: Calligonum canescens Pursh, Flora

Americae Septentrionalis 370. 1814. Atriplex canescens

(Pursh) Nutt., Genera of North American Plants 1:197.

1818.

Type collection: South Dakota: Lyman County, Big Bend

of the Missouri, Lewis on Sept. 21, 1804 (holotype PH).

Low shrubs or suffrutescent, spreading through root sprouting, sometimes to 20 x 20 m. Single-sex clones visible where

plants are sufficiently far apart, otherwise sexes intermingling. Leaves somewhat longer and narrower than those of

race Aptera, with which there may be some intergradation,

6-methoxy flavonols present.

Found on badlands and shale, mostly along the Missouri

River. Both race Aptera and race Canescens occur as localized, widely separated populations, and may have gained

their present distributions at a time of greater aridity, when

competition from grasses was less.

Race Cunescens (4x)

Taxonomic names: none.

Low shrubs, about 1–2 dm in height, resembling

Occidentalis, but with fruits having reduced or missing

wings fairly common, 6-methoxy flavonols present.

Found in Carbon and Emery Counties, Utah. Cunescens

may have arisen as a segregant from the hybridization

Occidentalis x Atriplex cuneata, the latter a common species

in the Colorado Plateau, and hence the name “Cunescens.”

Race Mexicana (4x)

Taxonomic names: none.

Bush size and leaf form are variable between populations,

although generally resembling race Occidentalis, 6-methoxy

flavonols absent.

The presence of Mexicana has been documented by flavonoid and chromosome number samples, from Entronque

San Roberto in southern Nuevo Leon, to at least as far as the

city of San Luis Potosi, but its distribution needs further

study. There appears to be wide morphological variation

between presently known locations, suggesting that it contains more than one phylogentic unit. Shorter forms may

have given rise to the hexaploid race Prostrata of southern

Nuevo Leon. Unlike the more northerly tetraploid Occidentalis, it exhibits a 6-methoxy flavonol negative flavonoid

pattern, like the Sonoran and Chihuahuan Desert higher

polyploids (table 1). It would, therefore, be a likely candidate

as their ancestor at the tetraploid level. Probably, tetraploids

of this flavonoid type were once somewhat more widespread,

but have been overwhelmed genetically by introgression

from Occidentalis.

Race Navajoensis (4x)

Taxonomic names: Atriplex navajoensis C. A. Hanson,

Studies in Systematic Botany 1: 3. 1962. Atriplex garrettii

var. navajoensis (C. A. Hanson) Welsh & Crompton, Great

Basin Naturalist 55: 326. 1995.

Type: Arizona: Coconino County, east side of Navajo

Bridge (abundant), C. A. Hanson 388(holotype BRY, isotypes

K, GH, POM, UC, US).

Low shrub to 0.5 m in height, usually 1–2 dm in height

exclusive of the inflorescence. Leaves to about 1 cm wide,

obovate to obcuneate, 6-methoxy flavonols variably present.

Found on the Vermillion cliffs of Coconino County, Arizona, for a few miles in each direction from Lee’s Ferry. As

suggested by the describer, this entity appears to have had

the hybrid origin Occidentalis x Garrettii. As would be

expected, there is a strong resemblance between Garrettii

and Navajoensis, and there is variation in the direction of

Garretti in Navajoensis populations near the Colorado River

at Lee’s Ferry (Stutz and Sanderson, unpublished data on

file at Brigham Young University). Hybridization with

Occidentalis continues at the present time at Lee’s Ferry.

Race Occidentalis (4x)

Taxonomic names: Pterochiton occidentale Torr. & Frem.,

Rep. exped. Rocky Mts. 318. 1845. Atriplex canescens var.

occidentalis (Torr. & Frem.) Welsh & Stutz, Great Basin

Naturalist 44: 188. 1984.

Type: Utah: “probably from the borders of the Great Salt

Lake,” Fremont in 1843 (holotype NY).

Woody shrub 0.75–1.5 (2) m in height, leaves linear

oblanceolate or linear ovate, the smaller often folded, apices

acute or obtuse. Distinctive winter foliage of small, reflexedappressed leaves occurring in many populations. Fruiting

beak small or absent, fruiting wings entire or somewhat

dentate, usually variable within a population, fruit usually

0.7–1.0 cm wide, 6-methoxy flavonols present.
82 USDA Forest Service Proceedings RMRS-P-21. 2001

Sanderson and Stutz Chromosome Races of Fourwing Saltbush (Atriplex canescens), Chenopodiaceae

This race is vigorous and widespread, occurring in the

Western United States and Northern Mexico. It tolerates a

variety of substrates, although sometimes demonstrating a

preference for sand. It has been reported that spreading by

root sprouts occurs in occasional plants in some New Mexican populations (Barrow 1997). Occidentalis plants are

erect, woody shrubs, in contrast to those of race Canescens

on the Missouri River. Plants of most populations of

Occidentalis resprout from the roots when cut off or burned,

but have not been otherwise observed to reproduce by

rootsprouting.

Race Diegensis (6x)

Taxonomic name: none.

Moderate to large shrubs, leafy. Foliage color greenish,

usually rather dark, pubescence relatively thin, 6-methoxy

flavonol positive.

All our chromosome counts for the Pacific Coast from Los

Angeles to the border between Baja California Norte and

Baja California Sur have been hexaploid, and flavonoid

samples have shown the plants to be 6-methoxy flavonol

positive. Flavonoid pattern and morphological similarity

would suggest a relationship of hexaploid Diegensis with the

widespread tetraploid race Occidentalis, or perhaps with

Angustifolia-4x or Vallis 6x. More study is needed regarding

distribution and characteristics of this race.

Race Nana (6x)

Taxonomic names: none.

Low shrubs, most often 2 dm tall or less, although sometimes taller, depending on genotype and moisture availability. Fruits small, 5–7 mm wide including wings, highly

variable within and between plants. Fruiting wings laciniate and often irregular with some of the wings incomplete or

with wing fragments growing in the areas between the

normal four wings, or wings in some individuals reduced to

small ridges on the fruit, or else absent, 6-methoxy flavonols

are produced in a minority of plants.

Nana occurs in southern Eureka and northern Nye Counties in Little Smokey Valley and in the Black Rock volcanic

area. Its enormous variability and its intermediacy between

Atriplex canescens and the suffrutescent species indicate it

is of hybrid origin. In comparing Nana to the two A canescens

races present in the area that might have participated in its

origin, failure to detect 6-methoxy flavonols in most plants

suggests Race Nevadensis (6x) as the fourwing saltbush

parent rather than Occidentalis (4x). The suffrutescent

parent of Nana might have been Atriplex falcata (2x, 4x) or

A. tridentata (4x, 6x). Wingless fruit variants mostly have

fruiting bracts that are toothed or have “shoulders,” ordinarily indicative of A. tridentata influence. However, there

is a widespread entity of apparent falcata-tridentata parentage in eastern Nevada (A. anomala, 6x) that may be a more

likely suffrutescent ancestor.

As noted in the key there is a population of plants similar

to some variants of Nana in Buena Vista Valley below

Unionville, Pershing County, that may be derived from the

hybridization Nevadensis x A. tridentata. DNA analysis

would be desirable to definitively determine origins of the

various hybrid taxa, including Bonnevillensis (4x), Nana

(6x), and A. nuttallii according to Stutz (6x).

The latter is not treated here because its fruits have only

irregular wing segments and tubercles, not four definite

wings. Flavonoids (consistently 6-methy flavonol positive)

would favor Occidentalis rather than Nevadensis as the

fourwing saltbush ancestor of A. nuttallii, while instances of

sympatry and intergradation by Atriplex tridentata would

suggest that species as another major contributor.

Race Nevadensis (6x)

Taxonomic name: none.

Shrub slightly smaller than Occidentalis, usually 3–6 dm

in height, fruiting wings usually more deeply toothed than

those of Occidentalis, primary (not clustered) leaves of the

male inflorescence usually 5–7 mm wide or more, in contrast

to those of Occidentalis in Nevada, which are more often less

than 5 mm in width, 6-methoxy flavonol negative.

Found in the borders of the Mojave Desert in western and

central Nevada. Occidentalis is found both to the north and

to the south of the zone occupied by Nevadensis. The flavonoid constitution of race Nevadensis suggests derivation

from the tetraploid race Mexicana, currently limited to

central Mexico, rather than from Occidentalis, the widespread tetraploid of northern Mexico and the Western United

States.

Race Occidentalis-6x (6x)

Taxonomic name: none.

Similar to Occidentalis (4x), but leaves wider.

Several isolated hexaploid populations are known from

southern Arizona and other areas. Since populations of

tetraploid Occidentalis frequently contain a few hexaploid

individuals, the formation of hexaploid populations from

these should take place readily. The relatively southern

distribution of hexaploid populations suggests they may be

inherently less cold tolerant than tetraploids. More study is

needed to compare Occidentalis-6x, Diegensis, and Vallis,

which in view of their 6-methoxy flavonol-positive flavonoid

patterns, are all related to Occidentalis (4x).

Race Prostrata (6x)

Taxonomic names: none.

Low plants hedged by heavy grazing, most only 1–2 cm in

height, but doubtlessly capable of growing somewhat taller under

more favorable circumstances, 6-methoxy flavonol negative.

Found in the valley of Entronque San Roberto and La Paz,

about 50 miles southbound from Saltillo on Mexico Federal

Highway 57. Prostrata usually grows with grasses, also very

close cropped. A similar to much taller tetraploid found in

the same valley and in other areas to the south is designated

“Mexicana.”

Race Rachelensis-6x (6x)

Taxonomic names: none.

Shrub, commonly 0.5 m in height or less. Primary inflorescence leaves do not seem to be retained into summer and
USDA Forest Service Proceedings RMRS-P-21. 2001 83

Chromosome Races of Fourwing Saltbush (Atriplex canescens), Chenopodiaceae Sanderson and Stutz

autumn as in Nevadensis, larger foliage leaves wider than

those of Occidentalis. Winter leaves also seem to be slightly

wider than those of Nevadensis when they are viewed side by

side, 6-methoxy flavonol positive.

Found on lower slopes in Sand Springs Valley, Lincoln

County, Nevada, where the town of Rachel is located (upper

slopes sometimes have Occidentalis). A possible origin for

this entity might be Rachelensis (8x) x Occidentalis (4x + 2x

= 6x). Rachelensis-6x closely resembles the octoploid except

that it is less gray-canescent. It grows a little above the

octoploid in the valley and is more abundant.

Race Tooelensis (6x)

Taxonomic names: none.

Shrubs to 0.5 m in height, leaves averaging wider than

those of tetraploid Occidentalis, 6-methoxy flavonol positive.

Found on both sides of Utah Highway 112 in a restricted

area between the towns of Tooele and Grantsville, Utah, it

is threatened by agriculture and urbanization. This is an

area of silt dunes that were active in producing dust storms

during the 1930s due to drought and overgrazing. The area

was rehabilitated by the CCC and planted with seeds of

Atriplex canescens, said to have come from a warehouse in

Colorado. It is possible that the seeds may have been mostly

those of race Vallis (6x). Tooelensis differs from Vallis in

flowering until late in the summer, and probably in its

climatic tolerances. It is observed to hybridize with Atriplex

tridentata (6x), which may, therefore, have contributed

genetically to its origin. A somewhat different possibility is

that Tooelensis was formed more anciently by hybridization

of Occidentalis and A tridentata. Presence of spontaneous

hexaploid individuals within Occidentalis could have allowed introgression of fourwing saltbush traits into an A.

tridentata population, which in an unusually favorable situation (namely, a very small population of A. tridentata

surrounded by abundant Occidentalis) could have driven

introgression far in the direction of fourwing saltbush. The

formation of mostly sterile pentaploid hybrids (2x + 3x = 5x),

from which occasional euploid derivatives at the hexaploid

or tetraploid levels might be expected (Stutz and others

1979), could have also contributed. Because the area of

occurrence was observed to be devoid of vegetation in the

1930s, origin from race Vallis seems more likely.

Race Vallis (6x)

Taxonomic names: none.

Shrubs, usually shorter than those of race Occidentalis,

often less than 0.5 m in height, flowering later than other

races in the same area, forming large stands. Leaves averaging wider than those of Occidentalis (4x), foliage appearing

slightly darker gray, 6-methoxy flavonol positive.

Found in bottomlands along the Rio Puerco, the Rio

Grande as far south as west Texas, and at the south of

White Sands and Alamogordo. There are also populations

appearing to be Vallis between Las Cruces, New Mexico,

and southeastern Arizona, but their chromosome number

in most cases has not been determined.

Vallis can easily be distinguished from other fourwing

saltbushes in central and southern New Mexico because of

its distinctively later flowering time (June rather than May).

Flavonoid composition would suggest a derivation from

Occidentalis.

Race Cuyamaensis (8x)

Taxonomic names: none.

Shrubs 1–2 m in height, leaves averaging larger than

those of Occidentalis, fruiting wings with large toothlike

lobes, 6-methoxy flavonol negative.

Found in lowlands near the river in Cuyama Valley, Kern

County, California. Occidentalis (4x) is also locally present

but seems to prefer slopes. Flavonoids suggest that

Cuyamaensis is not affiliated with Occidentalis, but with

Mexicana (4x), Nevadensis (6x), and the Mexican higher

polyploids.

Race Obtusifolia (8x)

Taxonomic names: Atriplex canescens var. obtusifolia

Sanderson & Stutz, var. nov.

Type: Mexico: Coahuila, 5 miles south of Cuatro Cienegas.

28 May 1980, Stutz 8573 (holotype BRY).

Atriplex prosopidium Johnston affinis sed statura minori,

foliis flavo-viride-pallidis non caeruleo-viridi-pallidis.

Shrubs 1–5 dm in height, leaves yellowish-green pallid

rather than bluish-green pallid as in Prosopidium, widely

oblanceolate to oblong, apically rounded to retuse, fruiting wings crenate to irregularly lobed, sometimes with

partial wings, or with wing fragments appearing between

normal wing positions, 6-methoxy flavonol positive.

Obtusifolia resembles race Prosopidium (Atriplex

prosopidium) to a considerable degree in leaf shape, but

differs from it in having a shorter stature, a greener, not

bluish foliage color, and in producing 6-methoxy flavonols.

Prosopidium from its type locality is 10x, but Prosopidium

plants from the valley of Monclova are 8x, like Obtusifolia.

The sometimes irregular fruits suggest hybridization, perhaps with the suffrutescent species A. obovata(6x, 6-methoxy

flavonol negative), but since A. obovata is 6-methoxy flavonol negative, 6-methoxy flavonoid production by Obtusifolia

would not be expected if those were the only parents.

Obtusifolia is found in bottomlands in the valley of Cuatro

Cienegas, Coahuila, where it forms a major element of the

vegetation.

Race Prosopidium-8x (8x)

Taxonomic names: see Prosopidium (10x).

Shrubs 5–12 dm in height, leaves small, relatively short

and broad, the larger usually 15–20 mm in length, apices

obtuse to retuse, foliage bluish-pallid, 6-methoxy flavonol

negative.

Found in the valley of Monclova. According to the descriptor, it is found mostly north of the city, growing in gypsiferous soils with Prosopis glandulosa. The occurrence of

Prosopidium-8x may have been reduced by urbanization

and agriculture.

A small and isolated 8x population was observed on the

west side of the valley that appeared intermediate with

Occidentalis. A cross between Occidentalis and 8x
84 USDA Forest Service Proceedings RMRS-P-21. 2001

Sanderson and Stutz Chromosome Races of Fourwing Saltbush (Atriplex canescens), Chenopodiaceae

Prosopidium might initially produce a hexaploid that, by

way of an unreduced gamete, could backcross to Occidentalis

to produce occasional progeny at the octoploid level, probably along with a lot of mostly sterile odd-ploids. The origin

of 8x Prosopidium might have been by the hybrid combination Mexicana x Atriplex obovata, the latter a 6-methoxy

flavonol negative suffrutescent species.

Race Rachelensis (8x)

Taxonomic names: none.

Shrubs 0.2–1 m in height, foliage heavily gray-furfuraceous, 6-methoxy flavonols present.

Found near the playa (dry lake bottom) in Sand Springs

Valley near Rachel. A very similar hexaploid is also present

at slightly greater elevations around the valley that is not as

gray. Both 6x and 8x Rachelensis have 6-methoxy flavonols,

suggesting the parentage of race Occidentalis. A possible

scenario is that the octoploid originated through hybridization between Nevadensis (6x) and Occidentalis (4x), both

found nearby, with an unreduced gamete from Nevadensis

(6x + 2x = 8x). Rachelensis-6x in turn might have been

generated from hybrids between Rachelensis (8x) and

Occidentalis (4x), by the combination of normal gametes

from each (4x + 2x = 6x).

Race Prosopidium (10x)

Taxonomic names: Atriplex canescens var. prosopidium

(Johnston) Sanderson & Stutz comb. nov. Atriplex

prosopidium Johnston, Journal of the Arnold Arboretum 24:

227. 1943.

Type: Mexico, Coahuila: south of El Oso, rounded bush 2–

3 ft tall, Johnston 8877 (holotype GH).

Shrubs 0.5–1.2 m in height, leaves oblanceolate to widely

oblanceolate or oblong-ovate, fruiting wings prominently

paucidentate.

Found in the southern part of the Valle las Calaveras,

which begins about 17 km North of the town of Cuatro

Cienegas, and also near the town of Sacramento, between

Cuatro Cienegas and Monclova. More study is desirable to

look for possible differences in morphology between 8x and

10x Prosopidium. Both were examined by the descriptor

(Johnston 1943). A possible origin for 10x Prosopidium

could have been the combination of a reduced with an

unreduced gamete within 8x Prosopidium to produce a 12-

ploid, followed by backcross to the 8x (4x + 8x = 12x; 6x + 4x

= 10x). Any further crossing would expectedly lead to

sterile products, but if isolated, 10x plants could cross

among themselves.

Race Laciniata (12x)

Taxonomic names: Atriplex canescens var. laciniata Parish, Flora of California 1: 442. 1914.

Type: California, Riverside County: Caleb (a town at the

southern end of the Salton Sea), Parish 8256 (holotype CAS,

isotype GH, photograph POM).

Large shrubs, 1–2 m in height, leaves usually up to 25

(30) mm in length, the apex commonly rounded. Fruits,

including wings up to 1.5 (2) cm wide, usually pedicellate,

the wings fimbriately or laciniately cleft or lobed, lobe tips

often appearing slightly swollen, fruiting beak with “shoulders” to 3-toothed, relatively inconspicuous, 6-methoxy

flavonols absent.

Found in California in the Sonoran and the western

Mojave Deserts and in northeastern Baja California Norte,

often on sand. Macilenta (12x) is similar, but with smaller

fruits. The dissected fruiting wings of Laciniata are suggestive of an origin by hybridization. The most apparent candidate would be Atriplex polycarpa (4x, 8x), except that it has

the wrong flavonoid composition (6-methoxy flavonol positive). Some other species might be possible but most of them

are diploid. The flavonoids of Laciniata (6-methoxy flavonol

negative) would suggest race Cuyamaensis (8x), Nevadensis

(6x), or Mexicana (4x) as the fourwing saltbush parent,

rather than Occidentalis.

Race Macilenta (12x)

Taxonomic names: Atriplex canescens var. macilenta

Jepson, Flora of California 1: 442. 1914.

Type: California, Imperial County: Bluffs of the Alamo,

Calexico, Parish 8258 (lectotype GH).

Medium shrubs, usually 0.5–1 m in height, leaves usually

up to 25 mm in length, the apex commonly rounded. Fruits

small, often like a laciniata fruit in miniature, width including wings about 5–7 mm, fruiting bracts fimbriately to

laciniately lobed, fruiting beak with “shoulders” to 3-toothed,

inconspicuous in comparison to the projections of the wings,

6-methoxy flavonols absent.

Found in the Sonoran Desert of California. Fruit and

shrub size vary from one place to another and intergrade

with Laciniata. Small fruit size and variability are suggestive of hybridization, but leaf shape does not suggest a

parent with leaves greatly different than those of Laciniata.

Two acceptable candidates might therefore be Atriplex

polycarpa (4x, 8x), which has A. canescens-like leaves in

wetter seasons, and race Linearis (2x). Atriplex polycarpa 8x

might have formed a 12-ploid via an unreduced gamete, and

the 12-ploid might then have hybridized readily with

Laciniata. In the case of Linearis, a mostly sterile 13-ploid

could be produced by union of an unreduced Laciniata

gamete plus a normal linearis gamete (12x + x = 13x), and

euploid gametes (6x) should then occasionally be produced

by segregation. Neither origin seems clearly satisfactory. On

the one hand, 6-methoxy flavonols are present in Atriplex

polycarpa, but not in Macilenta (nor Laciniata). On the

other, a very slight genetic contribution from Linearis would

hardly seem enough to change the fruit characteristics to the

extent seen in Macilenta, unless there was a gene of strong

effect involved or the introgression was long recurrent. If

Linearis was indeed involved, however, it might explain the

sometimes confusing similarity between Linearis and

Macilenta.

Race Laciniata-14x (14x)

Taxonomic names: see Laciniata (12x).

Large shrubs, fruits fimbriate to laciniate or coarsely

dentate, 6-methoxy flavonols absent.
USDA Forest Service Proceedings RMRS-P-21. 2001 85

Chromosome Races of Fourwing Saltbush (Atriplex canescens), Chenopodiaceae Sanderson and Stutz

Known from a few miles east of the Colorado River mouth

in westernmost Sonora to the resort town of Golfo de Santa

Clara, and perhaps further eastward. Because we did not

travel extensively in the Gran Desierto, distributions of

Laciniata-14x and Grandidentatum are incompletely known.

Race Grandidentatum (20x)

Taxonomic names: Atriplex canescensvar. grandidentatum

Sanderson & Stutz, American Journal of Botany 81: 1045-

1053. 1994.

Type: Mexico, Sonora: 25 km east of Puerto Peñasco,

Sanderson 93047(holotype BRY, isotype MEXU).

Large shrubs, larger leaves usually 15–60 mm in length,

slightly to moderately blue-green pallid, 5–10 mm in width,

apically obtuse to acute or occasionally emarginated, fruits

about 1–2 cm in width, including wings, large-toothed or

laciniate, 6-methoxy flavonols mainly absent.

Found along the upper Sonoran coast in the Desierto de

Altar and at least the western side of the Gran Desierto,

mostly on sand.

As noted in a previous publication (Sanderson and Stutz

1994), Grandidentatum has been observed to hybridize with

Atriplex polycarpa 8x. This may be the reason for small

amounts of 6-methoxy flavonols that can be occasionally

detected in Grandidentatum samples.

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Sanderson, S. C.; Stutz, H. C.; Stutz, M.; Roos, R. C. 1999. Chromosome races in Sarcobatus (Sarcobataceae, Caryophyllales). Great

Basin Naturalist. 59: 301–314.

Setoguchi, H.; Osawa, T. A.; Pintaud, J.-C.; Jaffré, T.; Veillon, J.-M.

1998. Phylogenetic relationships within Aurucariaceae based on

RBCL gene sequences. American Journal of Botany. 85: 1507–1516.

Soltis, P. S.; Soltis, D. E.; Weller, S. G.; Sakai, A. K.; Wagner, W. L.

1996. Molecular and phylogenetic analysis of the Hawaiian

endemics Shiedea and Alsinidendron (Caryophyllaceae). Systematic Botany. 21: 365–379.

Stebbins, G. L., Jr. 1971. Chromosomal evolution in higher plants.

London, England: Edward Arnold Ltd.

Stutz, H. C. 1978. Explosive evolution of perennial Atriplex in

Western America. Great Basin Naturalist Memoirs. 2: 161–168.

Stutz, H. C.; Melby, J. M.; Livingston, G. K. 1975. Evolutionary

studies of Atriplex: a relic gigas diploid population of Atriplex

canescens. American Journal of Botany. 62: 236–245.

Stutz, H. C.; Pope, L.; Sanderson, S. C. 1979. Evolutionary studies

of Atriplex: adaptive products from the natural hybrid 6n A.

tridentata x 4n A. canescens. American Journal of Botany. 66:

1181–1193.

Stutz, H. C.; Sanderson, S. C. 1979. The role of polyploidy in the

evolution of Atriplex canescens. In: Goodin, J. R.; Northington, D.

K., eds. Arid land plant resources. Lubbock, TX: Texas Tech

University, International Center for Arid and Semi-Arid Land

Studies: 615–621.

Stutz, H. C.; Sanderson, S. C. 1998. Taxonomic clarification of

Atriplex nuttallii (Chenopodiaceae) and its near relatives. Sida,

Contributions to Botany 18: 193–212.

Zohary, D.; Nur, U. 1959. Natural triploids in the orchard grass,

Dactylis glomerata L., polyploid complex and their significance

for gene flow from diploid to tetraploid levels. Evolution. 13:

311–317.
86 USDA Forest Service Proceedings RMRS-P-21. 2001

Sanderson and Stutz Chromosome Races of Fourwing Saltbush (Atriplex canescens), Chenopodiaceae

Preliminary Key to Fourwing Saltbush Races

1. Plants suffrutescent, stems dieing at the end of the season. Leaves linear to oblong or lanceolate, oblanceolate, the larger

often with several teeth along the margin and the margins wavy. El Bolson de Mapimi (Mapimi Basin), Coahuila, Mexico

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Stewartii (2x, 6-methoxy flavonol negative)

1. Plants usually shrubby. Leaf margin teeth very rare, or if more common, leaves roundish and often 1 cm or more wide

2. Leaves less than 5 times as long as broad, the larger usually 1 cm wide or more. Plants a bright yellowish green during

much of the year but green or gray-green during growth, less than 0.5 m in height, growing within a few miles of the

Colorado River in Utah or Arizona

3. Leaves ovate or obovate, mostly less than 3 times as long as broad. Found in drainages above Glenn Canyon Dam

in Utah and Arizona . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Garrettii (2x, 6-methoxy flavonol negative)

3. Leaves obovate to obcuneate, 2 to 4 times as long as broad and about 1 cm wide. Vermillion Cliffs near Lee’s Ferry,

Arizona . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Navajoensis (4x, 6-methoxy flavonol negative or positive)

2. Leaves narrower or smaller, plants usually larger. Atriplex canescens in the narrower sense, keyed by geographic area,

as follows:

Plants of the Pacific Northwest (4x only) . . . . . . . . . . . . . . . . . . . . . Race Occidentalis (4x, 6-methoxy flavonol positive)

Plants of the western Great Plains (4x only)

1. Aboveground stems short lived, plants usually 0.5 m or less in height. Strongly rootsprouting, individual clones often

covering many square meters. Found in South Dakota, especially along the Missouri River, on badland soils . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Canescens (4x, 6-methoxy flavonol positive)

1. Aboveground stems woody, persistent, most plants not spreading clonally

2. Fruit wings small, usually lobed, laciniate or irregular. Fruits including wings, 5–7 (10) mm wide or less. Low plants

with wide leaves. Alberta, Saskatchewan, Montana, North and South Dakota, Wyoming . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Race Aptera (4x, 6-methoxy flavonol positive)

2. Fruit wings normal in form and size, the margins entire to toothed. Fruits including wings about 7–10 mm wide. Mostly

Nebraska southward . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Occidentalis (4x, 6-methoxy flavonol positive)

Plants of Nevada or northern Arizona (2x, 4x, 6x, 8x)

1. Plants of Sand Springs Valley (near the town of Rachel), Lincoln County, Nevada

2. Larger leaves in the fall usually 5 mm or less in width. Plants of higher elevations around the valley edges, especially

along the highway approaching Rachael from the east . . . . . . . Race Occidentalis (4x, 6-methoxy flavonol positive)

2. Larger leaves in the fall usually more than 5 mm in width. Lower elevations

3. Gray-canescent plants of low elevations known from the area between the highway and the dry lake bed (playa) . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Rachelensis (8x, 6-methoxy flavonol positive)

3. Plants of similar appearance but not as gray, growing above the previous on lower valley slopes. Large populations

in some areas, especially north of the playa . . . . . . . . . . . . Race Rachelensis 6x (6x, 6-methoxy flavonol positive)

1. Plants of other areas

4. Length-width ratio of larger leaves about 10:1 or greater during most of the year

5. Plants growing at elevations of 1,500 m (5,000 ft) or greater in Lake Valley at Pioche, Lincoln County, also known

from the vicinity of Tuba City, Arizona . . . . . . . . . . . . . . . . . . . Race Piochensis (2x, 6-methoxy flavonol negative)

5. Plants at lower elevations or other locations. Known from Valley of Fire and Overton, Nevada, and scattered plants

in northern Arizona and northwestern New Mexico, intergrading with Occidentalis . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Angustifolia 4x (4x, 6-methoxy flavonol positive)

4. Length-width ratio of larger leaves usually below 10:1

6. Fruiting wings small, fruits to about 5 (7) mm in width including wings, deeply lobed, often irregular in size and

sometimes in position. Fruits strongly variable within and between plants, usually including some plants of a

population with a few wingless fruits. Found in southern Eureka, and northern Nye Counties. Plants growing in the

bottom of northern Buena Vista Valley, below Unionville, Pershing County, may have larger fruits but could perhaps

also be classified here. (Not included in the key, because it cannot be said to have four wings, but only wing fragments,

is the putative hybrid derivative Atriplex nuttallii, in the sense of Stutz (Stutz and Sanderson 1998), of the Humboldt

River valley and other locations in the Battle Mountain area) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . Race Nana (6x, mostly 6-methoxy flavonol negative, with occasional plants positive)

6. Fruiting wings normal in size, sometimes strongly dentate but extending the length of the fruit and growing in only

the four ordinary positions, fruits usually 7–10 mm in width

7. Larger leaves of the male inflorescence, when under 25 mm in length, 7 mm or more in width in the majority of

plants of a population. Anthers mostly 0.75 to 1.00 mm in length. Borders of the Mojave Desert in western and

central Nevada . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Nevadensis (6x, 6-methoxy flavonol negative)

7. Larger leaves of the male inflorescence usually less than 7 mm in width. Anthers usually 0.50 mm in length or

less. More generally distributed than Nevadensis (above), both to the north and south . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Occidentalis (4x, 6-methoxy flavonol positive)
USDA Forest Service Proceedings RMRS-P-21. 2001 87

Chromosome Races of Fourwing Saltbush (Atriplex canescens), Chenopodiaceae Sanderson and Stutz

Plants of Utah or western Colorado (2x, 4x, 6x)

1. Length-width ratio of larger summer leaves 10:1 or greater. Plants of the Little Sahara Dunes, Juab County, Utah . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Gigantea (2x, 6-methoxy flavonol negative)

Length-width ratio of larger summer leaves less than 10:1

3. Fruiting wings small and irregular or occasionally absent, fruits, including wings usually 5 (7) mm or less in width.

Known from Juab and Millard Counties of western Utah . . . . . . . Race Bonnevillensis (4x, 6-methoxy flavonol positive)

3. Fruiting wings sometimes small or more often normal in size, usually entire to moderately toothed. Fruits, including

wings usually 7–10 mm wide

4. Plants of Tooele County, Utah, between the towns of Tooele and Grantsville on the north and south sides of Utah

Highway 112, about 2 miles east of Grantsville. Grayish, shorter plants with wider leaves, flowering until late

summer (plants closer to Grantsville are race Occidentalis) . . Race Tooelensis (6x, 6-methoxy flavonol positive)

4. Plants widespread or of other areas

5. Plants mostly about 2 dm in height or less, of Carbon or Emery County, Utah . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Cunescens (4x, 6-methoxy flavonol positive)

5. Plants averaging well over 2 dm in height. Widespread . . . . . Race Occidentalis (4x, 6-methoxy flavonol positive)

Plants of New Mexico, or San Luis Valley, southern Colorado (2x, 4x, 6x)

1. Plants of San Luis Valley, Colorado, or Taos County, New Mexico

2. Plants generally over 0.5 m in height . . . . . . . . . . . . . . . . . . . . . . . . Race Occidentalis (4x, 6-methoxy flavonol positive)

2. Plants mostly about 0.5 m or less in height

3. Width of largest summer leaves 2–3 mm during seasons of drought, foliage usually yellowish. Occurring west of the

Rio Grande in Taos County, New Mexico, and south of Antonito in Conejos County, Colorado . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Brevis (2x, 6-methoxy flavonol negative)

3. Width of larger leaves usually about 5 mm or greater except in winter, foliage more greenish. More widespread than

the previous . . . . . . . . . . . . . . . . . . . . . . . . . . . Occidentalis x Brevis introgressants (4x, 6-methxy flavonol positive)

1. Plants not of San Luis Valley or Taos County, New Mexico

4. Length-width ratio of larger leaves about 10 or greater

5. Larger leaves at some seasons only 2–3 mm in width in most populations, foliage with a pronounced yellowish color

in dry hot seasons. Typically growing on sand dunes or mesquite hummocks, usually on uplands above tetraploids

and hexaploids; however, mixed 2x-4x populations are rather common in the Rio Grande Valley . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Angustifolia (2x, 6-methoxy flavonol negative)

5. Larger leaves usually wider than 2–3 mm at all seasons, foliage color not as yellow. Leaf length-width ratio not much

exceeding 10:1, usually less at some seasons. Occurring on a variety of substrates . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Angustifolia-4x (4x, 6-methoxy flavonol positive)

4. Leaf length width ratio less than 10, larger leaves wider than 2–3 mm during all seasons. Foliage more consistently

grayish during all seasons

6. Plants with new flowers appearing only in June, if not of northern New Mexico. Low bottomland plants of a slightly

darkish foliage color . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Vallis (6x, 6-methoxy flavonol positive)

6. Plants with new flowers appearing in May, except at higher elevations in the north. Larger plants, often occurring

on slopes, with a somewhat more yellowish dry-season foliage color than the previous . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Occidentalis (4x, 6-methoxy flavonol positive)

Plants of California, southern Arizona, Baja California, or Sonora (2x, 4x, 6x, 8x, 12x, 14x, 20x)

1. Length-width ratio of larger leaves about 10:1 or greater

2. Fruits with small or irregular wings, width, including wings usually 5 (10) mm or less. Bottomland plants, the foliage

usually with a slight bluish cast. Fruits usually not pedicellate, but prominently beaked . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Linearis (2x, 6-methoxy flavonol negative)

2. Fruit with well developed wings, width including wings usually 7–10 mm or more. Plants usually of well-drained sites,

fruits pedicellate, fruiting beaks usually obscure or absent

3. Plants of Imperial Valley, California, and the western Sonoran and Mojave Deserts . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Angustifolia-4x (4x, 6-methoxy flavonol positive)

3. Plants of the Arizona portion of the Sonoran Desert, especially south of Tucson . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Angustifolia (2x, 6-methoxy flavonol negative)

1. Length-width ratio of larger leaves mostly less than 10:1

4. Fruit wings usually entire to moderately toothed

5. Plants of the Pacific Coast of Baja California Norte and California, below Los Angeles . . . . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Diegensis (6x, 6-methoxy flavonol positive)

5. Plants of other areas

6. Leaves narrower at a given season. Plants widespread . . . Race Occidentalis (4x, 6-methoxy flavonol positive)

6. Leaves wider by comparison. Isolated populations . . . . . . Race Occidentalis-6x (6x, 6-methoxy flavonol positive)

4. Fruiting wings of all or most plants having large teeth, or prominently lobed or incised
88 USDA Forest Service Proceedings RMRS-P-21. 2001

Sanderson and Stutz Chromosome Races of Fourwing Saltbush (Atriplex canescens), Chenopodiaceae

6. Plants of Cuyama valley, California, mostly in bottomlands. Fruiting wings with large irregular teeth. (Occidentalis

present in the general locality also, on slopes) . . . . . . . . . . . Race Cuyamaensis (8x, 6-methoxy flavonol negative)

6. Plants of the southern Mojave or Sonoran Deserts

7. Southern California and Baja California Norte

8. Plants usually 1 m in height or more, fruiting bracts normal to large in size, fruits about 7–15 (20) mm in width

including wings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Laciniata (12x, 6-methoxy flavonol negative)

8. Plants usually less than 1 m in height, fruiting bracts small, fruit usually 5–7 (10) mm or less in width, including

wings

9. Plants normally 0.5 m in height or less, fruits mostly sessile, foliage with a bluish cast in the field (a few

populations with wider leaves will key out here) . . . . . . . . Race Linearis (2x, 6-methoxy flavonol negative)

9. Plants mostly greater than 0.5 m in height, fruits mostly pedicellate, foliage often pale, but greenish.

Apparently intergrading with Laciniata . . . . . . . . . . . . . . . . . Race Macilenta(12x, 6-methoxy flavonol negative)

7. Coastal northern Sonora

10. West of Gran Desierto . . . . . . . . . . . . . . . . . . . . . . . . Race Laciniata 14x (14x, 6-methoxy flavonol negative)

10. Gran Desierto(?) and Desierto de Altar . . . . . . . . . . Race Grandidentatum (20x, 6-methoxy flavonol negative)

Plants of the Chihuahuan Desert of Mexico (2x, 4x, 6x, 8x, 10x)

1. Length-width ratio of larger leaves 10:1 or more, larger leaves during dry seasons usually 2–3 mm in width or less, dry

season foliage color markedly yellowish. . . . . . . . . . . . . . . . . . . . . Race Angustifolia (2x, 6-methoxy flavonol negative)

1. Length-width ratio of larger leaves usually less than 10:1, larger leaves, even during drier seasons, usually over 2–3 mm

in width. Foliage color not as strongly yellowish

2. Foliage bluish-green pallid, leaf apices usually rounded, leaves short and fairly wide

3. Plants of Coahuila

4. Plants of Valle Las Calaveras, between the towns of Ocampo and Cuatro Cienegas, or at Sacramento, Coahuila.

Pure large stands (where not extirpated by agriculture) or growing with Race Occidentalis . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Prosopidium (10x, 6-methoxy flavonol negative)

4. Plants of the valley of Monclova, Coahuila . . . . . . . . . . Race Prosopidium-8x (8x, 6-methoxy flavonol negative)

3. Plants of Chihuahua . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Prosopidium? (6x, 6-methoxy flavonol status unknown)

2. Foliage grayish-green or yellowish-green pallid, leaf apices rounded or not

5. Plants of the valley of Cuatro Cienegas, Coahuila. Leaf apices rounded, leaves relatively short and wide, plants

usually below 0.5 m in height, forming large uniform stands. Differing from races of Prosopidium by shorter stature

and non-bluish foliage color . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Obtusifolia (8x, 6-methoxy flavonol positive)

5. Plants widespread or of other localities, leaves not particularly short and wide

6. Plants of southern Nuevo Leon or San Luis Potosi

7. Plants 2 or 3 dm in height or less, most often only a few cm, growing in the valley bottom from Ent. San Roberto

for about 20 km northward . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Prostrata (6x, 6-methoxy flavonol negative)

7. Plants of various populations ranging in stature from very low like Prostrata to much taller, growing from La

Paz southward to about 20 km north of Ent. San Roberto, and from San Roberto to at least as far as the city of

San Luis Potosi. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Mexicana (4x, 6-methoxy flavonol negative)

6. Plants more northern . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Race Occidentalis (4x, 6-methoxy flavonol positive)
USDA Forest Service Proceedings RMRS-P-21. 2001 89

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Brian D. Vanden Heuvel is a Graduate Student at the University of Texas

at Austin, Section of Intergrative Biology, Austin, TX 78712. C. Randal Linder

is an Assistant Professor, Section of Intergrative Biology, Austin, TX 78712.

A Molecular Phylogeny for Cercocarpus

H.B.K. (Rosaceae) Using the External

Transcribed Spacer of the Nuclear

Ribosomal Repeat

Brian D. Vanden Heuvel

C. Randal Linder

Abstract—Cercocarpus H.B.K. (Rosaceae) taxa are important

members of the plant communities of the western states and Mexico,

yet the systematics of this genus are unknown primarily from lack

of clear morphological delimitations between taxa. In recent years,

molecular data have proven useful for resolving relationships among

species and the diversity within species that have otherwise remained elusive. We will report here preliminary data on the phylogenetic utility of two noncoding regions within the nuclear ribosomal DNA (nrDNA) for Cercocarpus; the internal transcribed spacer

(ITS) region and the external transcribed spacer (ETS) region. The

ITS and ETS were amplified and sequenced in five individuals

representing four Cercocarpus taxa. Maximum parsimony and

maximum likelihood phylogenies were created from the two aligned

data sets and compared. We found that the ETS has considerably

more phylogenetically informative sequence variation than the ITS,

which had almost no signal. Further sampling of ETS sequences in

Cercocarpus taxa produced four main ETS types. The four ETS

types were alignable only in the extreme 5’ and 3’ regions of the ETS

sequence. Large regions of the ETS sequences were unalignable

between different ETS types. Phylogenetic analysis of a reduced

data set including just the regions in common between ETS types

suggest that the different ETS types in Cercocarpus diverged prior

to the origin of the genus, making them paralogous. This deep

coalescence requires that a single ETS type be used for reconstruction.

Introduction ____________________

Cercocarpus H.B.K. (Rosaceae) is a New World genus

composed of montane xerophytic shrubs and trees, found in

deserts, chaparral, and mountainous regions of western

North America with a center of diversity in northern Mexico.

Botanists have paid attention to the ecology and management of Cercocarpus in the United States because the

evergreen leaves found on most members of the genus have

high levels of protein and are an important winter forage for

wildlife and livestock in western states (Blauer and others

1975; Davis and Brotherson 1991).

The systematics of Cercocarpus are largely unknown; the

genus lacks a consensus classification or phylogeny. Since it

was first described, Cercocarpus has undergone three revisions (Schneider 1905; Rydberg 1913; Martin 1950), each

varying widely in the ranks assigned to taxa and the number

of species. Much of the current taxonomy of Cercocarpus is

based on quantitative characteristics involving leaf morphology (Schneider 1905; Rydberg 1913; Martin 1950). Confusion about the number and circumscription of species

within Cercocarpus arises primarily from the lack of clear

morphological delimitations between taxa. Variations in

leaf morphology show a continuum within and between

taxa, making it difficult to define boundaries among species

(Brayton and Mooney 1966; Mortenson 1973). A phylogeny

based on leaf characters is poorly supported due to severe

homoplasy.

In recent years, molecular data have proved useful for

resolving relationships among morphologically similar species and for understanding the diversity within species

(Soltis and Soltis 1998 and references therein). A phylogeny

and a clear definition of taxa using molecular markers

within Cercocarpus is critical to an understanding of the

evolution and systematics of Cercocarpus. Knowledge of the

systematics of Cerocarpus may enhance its breeding and

help prevent undesirable hybridization of species and

ecotypes planted in reclaimed areas using bulk seed.

We report here preliminary results on the phylogenetic

utility of two noncoding regions within the 18S-26S nuclear

ribosomal DNA (nrDNA) repeat for Cercocarpus: the internal transcribed spacer (ITS) region and the external transcribed spacer (ETS) region (fig. 1). Both the ITS region and

Figure 1—Representation of the 18S-26S ribosomal repeat in the nuclear genome. The genes

(26S, 5.8S, and 18S) are shown by the large

boxes. Transcription begins at the TIS. Both the

ETS and both ITS regions are removed after

transcription. The general location and direction

of the primers used in this study are shown by

arrows and italized text.
90 USDA Forest Service Proceedings RMRS-P-21. 2001

Vanden Heuvel and Linder A Molecular Phylogeny for Cercocarpus H.B.K. (Rosaceae) Using the External Transcribed Spacer of the Nuclear Ribosomal Repeat

the ETS region have been used with success in phylogenetic

reconstruction at the generic and specific level in other plant

groups (for example, Baldwin 1995; Bena 1998; Baldwin and

Markos 1998; Linder and others 2000). Recently, the ETS

has been shown to contain informative variation in groups

where ITS does not (Bena 1998; Baldwin and Markos 1998;

Linder and others 2000).

Materials and Methods ___________

Taxon Sampling

For this report, we follow the taxonomy of Martin (1950)

with the exception of the Mexican taxa, for which we turned

to an unpublished treatment by J. Henrickson (personal

communication). Twenty-six taxa were sampled (table 1). In

six cases more than a single individual represented a taxon.

For each sample, DNA was extracted from the collections

using a modified CTAB procedure (Doyle and Doyle 1987).

Genomic DNA extractions were cleaned using the Elu-quik

DNA purification kit (Schleicher and Schuell) prior to PCR

amplification.

Amplification, Sequencing, and Analysis

of the ITS Region

To test the phylogenetic utility of the ITS region in

Cercocarpus, we selected five individuals representing four

exemplar taxa of Cercocarpus (table 1). This sampling

strategy was designed to compare the amount of variation

observed between very closely related individuals (two individuals of C. montanus var. montanus) and more distantly

related taxa, as determined by recent work on the leaf

architecture of Cercocarpus by Lis (1992). The ITS region

was amplified using the primers ITS 5 and ITS 4 (Innis and

others 1990). A negative control was also used that lacked

template DNA. Fifty microliter PCRs were performed using

30mM Tricine, pH 8.4, 2mM MgCl2, 50 mM KCl, 5 percent

acetamide, 100 uM of each dNTP, 1.0 unit of Taq polymerase, and 30 nM of each amplification primer. Twenty ng

of template DNA was added and the reactions were overlaid

with mineral oil and run on an MJ Research Thermal Cycler

programmed for a hot start (95 °C, 5 min; 74 °C, 7 min) and

30 cycles of 94 °C for 30 sec, 50 °C for 45 sec, and 72 °C for

1 min. A final extension of 72 °C for 7 min was also included.

Table 1—Collection and ETS type data for the 26 populations of Cercocarpus and Purshia analyzed. Collectors: JH-James

Henrickson, BVH-Brian Vanden Heuvel, BC-Bonnie Crozier. Vouchers are housed at the University of Texas (TEX).

Taxon Population no. Collection location and number ETS type(s)

C. montanus var. montanus 5a Douglas Co., CO BVH 5 1

8 Platte Co., WY BVH 8 1

10a Custer Co., SD BVH 10 1

C. montanus var. glaber 12 Brewster Co., TX JH 20663 1

14 Brewster Co., TX JH 20665 1

15 Brewster Co., TX JH 20666 1

16 Brewster Co., TX JH 20667 1

17a Coahuila, MX JH 20439b 1

C. montanus var. paucidentatus 1 Tamaulipas, MX JH 19218 1

27C Eddy Co., NM BVH 27 1

C. montanus var. blancheae 19 Los Angeles Co., CA BVH 123a 2

20 Los Angeles Co., CA BVH 123b 2

21 Los Angeles Co., CA BVH 123c 2

62D Tulare Co., CA BVH 127a 1

65C Tulare Co., CA BVH 127b 2

65D Tulare Co., CA BVH 127c 1

C. montanus var. traskiae 52B Los Angelas Co., CA JH 22312 2

C. montanus var. minutiflorus 57 San Diego Co., CA JH 22311 1, 2

C. fothergilloides var. mojadensis 18a Coahuila, MX JH 13156 2

66 Coahuila, MX BVH and JH 11824 3

C. fothergilloides var. medranoanus 82 Tamaulipas, MX BVH and JH 22444 1, 3

C. macrophyllus 26 Coahuila, MX BC 1034 1, 2

C. rzedowskii 78 Tamaulipas, MX BVH and JH 22446 1

81 Tamaulipas, MX BVH and JH 22460 4

C. ledifolius var. intermontanus 45 Box Elder Co., UT BVH 45 1

C. ledifolius var. ledifolius 41 Emery Co., UT BVH 41 1

C. ledifolius var. intricatus 25a Garfield Co., UT BVH 45 1

Purshia tridentata 34 La Plata Co., CO BVH 34

a

Individuals for which the ITS and ETS were compared.
USDA Forest Service Proceedings RMRS-P-21. 2001 91

A Molecular Phylogeny for Cercocarpus H.B.K. (Rosaceae) Using the External Transcribed Spacer of the Nuclear Ribosomal Repeat Vanden Heuvel and Linder

Three uL of the reaction mixture was run on a 1.5 percent

agarose gel in a 0.5X TBE buffer. PCR products were visualized with ethidium bromide under UV light. PCR products

were purified (QIAquick PCR purification kit, QIAGEN)

and sequenced on an ABI Prism 377 automated sequencer

using standard reagents at the Core Facility of the Molecular Biology Institute at the University of Texas. Sequences

were proofread and then aligned using Clustal W in MegAlign

(DNAstar, 1998), followed by adjustment by eye. Aligned

ITS sequence data was used to generate phylogenetic trees

in PAUP 4.0.0d64 (kindly provided by David Swofford).

Gaps were treated as missing data. Trees were constructed

using maximum likelihood and maximum parsimony algorithms with the exhaustive search option. The specific

parameters for the ML analysis were unequal transitiontransversion rates and empirically determined nucleotide

frequencies. Support for the monophyly of groups was

evaluated using bootstraping (Felsenstein 1985).

Developing the ETS in Cercocarpus

To develop the ETS region for phylogenetic reconstruction

in Cercocarpus, we amplified the entire intragenic spacer

(IGS) of C. montanus (collection #5) and C. intricatus (collection #25) (table 1) using the primers 1M and 18S-2L((Linder

and others 2000)) present in conserved regions of the 26S

and 18S genes, respectively (fig. 1), and following the same

PCR parameters listed above except an extension time of

2 min. per cycle. We sequenced from the 3’ end of the amplified

product in both taxa following the same procedures as for the

ITS regions. Because the ETS region was too long to sequence

with a single primer, we developed internal primers to sequence through the transcription initiation site (TIS). We

identified the TIS based on similarity with the TISs in other

plant groups. As a result of its role in transcription of the rDNA

repeat, the TIS is under strong selection to stay conserved,

making it a good choice for priming throughout Cercocarpus.

We designed Cerc-ETS1f (5’-tataaaggggaggcctcatt-3’) to include the TIS and have high sequence similarity to both taxa

(fig. 1). Using this primer in combination with 18S-2L, we

amplified the ETS reliably for all Cercocarpus taxa from

which DNA was extracted from fresh material.

The ETS sequence for Purshia tridentata, used as the

outgroup for this study, was obtained by amplifying the

whole IGS as described above for Cercocarpus. We then

sequenced from the 3’ end of the amplified product until we

identified the TIS.

For each Cercocarpus taxon, one of two strategies was

conducted for sequencing the ETS. If the ETS amplification

produced a single PCR product, the product was sequenced

directly as outlined in the above section. If the ETS amplification produced multiple-length PCR products, we cloned

the PCR products using the TOPO-TA cloning kit (Invitrogen).

At least 10 colonies were screed for the ETS insert by direct

PCR amplification using the same PCR parameters except a

10 min. hot start at 95 °C to lyse the cells. At least two of

these amplifications were sequenced for each individual for

each ETS length variant.

Comparison of the Phylogenetic Utility of

the ITS and the ETS in Cercocarpus

The ETS sequences from the same five Cercocarpus individuals sampled to test the phylogenetic utility of the ITS

were proofread and aligned using Clustal W in MegAlign

(DNAstar 1998), followed by adjustment by eye. The five

ETS sequences consisted of four ETS type 1 sequences and

one ETS type 2 sequence (table 1, fig. 2). Only the 5’ and 3’

common regions of the ETS sequences (see Reults) were

included in the analyses (fig. 2). Maximum parsimony and

maximum likelihood analyses were carried out in PAUP

4.0.0d64 as described for ITS.

Alignment and Phylogenetic Analysis of

the ETS Types

All ETS sequences, regardless of type, were aligned using

Clustal W followed by adjustment by eye. Only regions of the

ETS sequences that were alignable between different ETS

types were included in the analyses (fig. 2). For ETS type 3

sequences, only the 5’ common region was included in the

aligned sequence matrix. Only the 3’ common region of the

ETS sequence of P. tridentata was included to serve as the

outgroup (fig. 2). Therefore, ETS type 3 sequences placement in the phylogeny is based only on its relationship to the

200 bp

5' Alignable region of the

ETS

Unalignable regions

between types of ETS

ETS type 1

(1000 bp)

ETS type 2

(800 bp)

Cerc-ETS1f ETS 18S-2L

18S

18S

ETS type 3

(750 bp)

18S

160 bp

18S

18S

ETS type 4

(500 bp)

Purshia ETS

type

(1300 bp)

3' Alignable region of the

ETS

Figure 2—Representation of all four ETS types found

in Cercocarpus to date and the ETS found in Purshia

tridentata. Representations begin at the transcription

initiation site (TIS) and go to the 18S gene. The

hatched boxes indicate the 5’ region that is alignable

among ETS types. The black boxes show the location

of the 3’ region that is alignable among ETS types.
92 USDA Forest Service Proceedings RMRS-P-21. 2001

Vanden Heuvel and Linder A Molecular Phylogeny for Cercocarpus H.B.K. (Rosaceae) Using the External Transcribed Spacer of the Nuclear Ribosomal Repeat

other ETS types and not on a direct comparison to the

outgroup. The resulting sequence matrix totaled 300 aligned

base pairs. Maximum parsimony and maximum likelihood

analyses were carried out in PAUP 4.0.0d64 as described for

ITS.

Results ________________________

Identification of Four ETS Types in

Cercocarpus

Amplification and sequencing of the ETS region using the

primers Cerc-ETS1f and 18S-2L resulted in the identification of four distinct ETSs (table 1, fig. 2). The different ETS

types ranged from 1,000 bp to 500 bp in Cercocarpus and was

1,300 bp in the outgroup Purshia. Three Cercocarpus individuals were found to contain multiple ETS types, 16 individuals had ETS type 1 only, four individuals had ETS type

2 only, one individual had ETS type 3 only, and one individual had ETS type 4 only (table 1).

Comparison of the ITS and the ETS

Regions

The ITS tree was based on an alignment of 700 bp, which

included the ITS1, ITS2, and 5.8S gene (fig. 1). ML and MP

analyses produced the same tree topology. Only the MP

results are presented here (fig. 3). The MP ITS tree had a

length of 2 and very weak bootstrap support for internal

branches due to lack of phylogenetically informative variation in the ITS region for the five individuals sampled.

The ETS tree for the same five individuals was based on

360 bp of aligned sequence data in the 5’ and 3’ common

regions (fig. 3). ML and MP resulted in the same tree

topology so only the MP results are presented (fig. 3). The

ETS tree had a length of 20 steps and considerably higher

bootstrap support for internal branches.

Figure 3—A comparison of MP phylogenies produced from 700 bp of aligned ITS sequences and

360 bp of aligned ETS sequence data. Numbers

above branches are the numbers of steps, numbers

below are bootstrap values.

Phylogenetic Analysis Using the ETS

The MP analysis of 5’ and 3’ common regions (360 bp) of 26

individuals of Cercocarpus and one individual of Purshia

tridentata resulted in over 10,000 equally parsimonious

trees of length 176. Figure 4 is a 50 percent majority rule

consensus tree based upon those trees. Each ETS type

formed its own clade, indicating the evolution of the types

prior to the origin of the genus. Further, each of the multiple

ETS types in C. montanus var. minutiflorus (pop. 57),

C. fothergilloidesvar. medranoanus(pop. 82), and C. macrophyllus (pop. 26) belonged to their respective “type” clade (fig. 4).

ETS type 1 sequences form a well supported clade, which is

Figure 4—Fifty percent majority rule maximum

parsimony consensus tree produced from the 360

bp alignment of the common regions between ETS

types. The dark grey box indicates the monophyly

of the ETS type 1 sequences, the light grey box

indicates ETS sequences of type 2, the white box

indicates the monophyly of ETS type 3 sequences,

and the black box indicates the placement of the

ETS type 4 sequence. Numbers below the branches

indicate bootstrap support.

montanus var. montanus 5

montanus var. montanus 8

montanus var. montanus 10

montanus var. glaber 12

montanus var. glaber 15

fothergilloides var. medranoanus 82

montanus var. glaber 14

montanus var. glaber 3

montanus var. paucidentatus 1

montanus var. glaber 16

montanus var. paucidentatus 27C

montanus var. paucidentatus 27C

ledifolius var. intermontanus 45

macrophyllus 26

rzedowskii 78

rzedowskii 78

ledifolius var. intricatus 25

ledifolius var. ledifolius 41

montanus var. blancheae 62D

montanus var. blancheae 65D

montanus var. blancheae 65D

montanus var. blancheae 62D

montanus var. traskiae 52B

fothergilloides var. mojadensis

macrophyllus 26

montanus var. blancheae 19

montanus var. blancheae 20

montanus var. blancheae 21

montanus var. minutiflorus 57

montanus var. minutiflorus 57

montanus var. blancheae 65C

montanus var. blancheae 65C

fothergilloides var. mojadensis 66

fothergilloides var. medranoanus 82

rzedowskii 81

Purshia glandulosa

18

ETS type 1

ETS type 2

ETS type 3

ETS type 4

C. montanus var. montanus

C. montanus var. montanus

C. montanus var. glaber

C. ledifolius var. intricatus

C. fothergilloides 13

C. montanus var. montanus

C. montanus var. montanus

C. montanus var. glaber

C. ledifolius var. intricatus

C. fothergilloides

Purshia tridentata
USDA Forest Service Proceedings RMRS-P-21. 2001 93

A Molecular Phylogeny for Cercocarpus H.B.K. (Rosaceae) Using the External Transcribed Spacer of the Nuclear Ribosomal Repeat Vanden Heuvel and Linder

sister to a clade containing ETS types 2, 3, and 4. Because

ETS type 3 sequences lack a 3’ common region and the

outgroup (P. tridentata) sequence lacks 5’ common region,

placement of ETS type 3 sequences in the phylogeny is based

on comparison to the other Cercocarpus ETS sequences and

not to direct comparison to the outgroup (fig. 2). ETS type 1

sequences form a well supported clade, which is sister to a

clade containing ETS type 2, 3, and 4 sequences.

Discussion _____________________

Comparison of the ITS and the ETS

Regions in Cercocarpus

The ITS region has been very attractive for phylogenetic

reconstruction in plants because it evolves rapidly, it is

subject to concerted evolution, and it is easily amplified

using universal primers in the flanking genes (Baldwin and

others 1995). However, in some studies of recently evolved

plant lineages, the ITS region lacks enough phylogenetically

informative variation to resolve relationships (Bain and

Jansen 1995; Baldwin and others 1995; Francisco-Ortega

and others 1997; Schilling and others 1998; Soltis and

Kuzoff 1993). This lack of variation in the ITS in some plant

groups (Fabaceae and Asteraceae) has led some researchers

to look at the ETS for more variation (Bena 1998; Baldwin

and Markos 1998; Linder and others 2000). Our results

indicate that the ETS is also more phylogenetically informative than the ITS in Cercocarpus (Rosaceae). The length of

the MP tree increased tenfold from 2 steps for the ITS tree

to 20 steps for the ETS tree, even though the aligned ETS

sequence data had only half the number of aligned base pairs

as the ITS (fig. 3). Also, the bootstrap support for internal

nodes increased dramatically in the ETS tree. Our results

add to those of others (Bena and others 1998; Baldwin and

Markos 1998; Linder and others 2000) that indicate that the

ETS can be more phylogenetically useful for resolving the

relationships of recently evolved taxa.

So little informative variation in the ITS for Cercocarpus

adds weight to claims that Cercocarpus is a recently evolved

group (Martin 1950), because there hasn’t been enough time

for variation to accumulate in the ITS. Recent origin of

Cercocarpus would explain why there has been such disagreement in the taxonomy and circumscription of taxa

(Schneider 1905; Rydberg 1913; Martin 1950).

Multiple ETS Types and Phylogenetic

Analysis Using the ETS in Cercocarpus

Multiple ETS types have been found in other plant groups,

including three genera in the Asteraceae: Asteriscus,

Calycadenia, and Helianthus (Baldwin and Markos 1998;

Linder and others 2000). However, the multiple ETS types

found in these genera only differed in numbers of sub-repeats

and did not show such large scale structural differences. The

large structural differences found among the ETS types in

Cercocarpus may be the result of past DNA mispairing events

during replication due to secondary structure. We are currently

cloning the ETS from genomic DNA obtained from different

Cercocarpus individuals with known ETS types to further

explore the molecular evolution of the ETS in Cercocarpus.

In an earlier study where multiple ETS types were found

in individuals (Linder and others 2000), the types were all

found to have originated within a species. There was no

evidence for deep coalescence of the types. In Cercocarpus,

we have found evidence for ETS types that have coalescence

times earlier than the origination of the genus. ETS types 1,

3, and 4 are monophyletic groups, and ETS type 2 is a very

closely related paraphyletic group. This is surprising because concerted evolution of the 18S-26S nrDNA repeat has

commonly been invoked to reduce or eliminate the effects of

deep coalescence on phylogenetic reconstruction (Moritz

and Hillis 1996; Zimmer and others 1980). Within Cercocarpus, lack of concerted evolution or lineage sorting followed

by hybridization has produced patterns of relationship that

do not fit the usual pattern. We do not have enough data to

tell which of these scenarios is more likely. In either case, the

data suggest that the ETS types are paralogous with an

ancient coalescence time. Different Cercocarpus ETS types,

therefore, should not be used together for phylogenetic

analysis. No problem should arise if a single ETS type is used

for phylogenetic reconstruction. We believe that, with more

sampling, a phylogeny using ETS type 1 will produce a usable

nuclear phylogeny for Cercocarpus. ETS type 1 was found in

all Cercocarpus taxa except C. montanus var. traskiae and

C. fothergilloides var. mojadensis (table 1). Continued sampling of these two taxa may discover usable ETS type 1

sequences to include in the phylogenetic reconstruction.

References _____________________

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aureoid Senecio (Asteraceae) complex based on ITS sequence

data. Plant Systematics and Evolution 195: 209–219.

Baldwin, B. G.; Sanderson, M. J.; Porter, J. M.; Wojciechowski,

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Vanden Heuvel and Linder A Molecular Phylogeny for Cercocarpus H.B.K. (Rosaceae) Using the External Transcribed Spacer of the Nuclear Ribosomal Repeat

low taxonomic levels in Asteraceae and closely allied families.

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nuclear ribosomal DNA internal transcribed spacer region sequence data. Systematic Botany 23: 177–187.

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USDA Forest Service Proceedings RMRS-P-21. 2001 95

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Alisa P. Ramakrishnan is a Masters Student in the Botany Department at

Brigham Young University, Provo, UT 84602. Craig E. Coleman and Daniel

J. Fairbanks are Professsors in the Botany Department, Brigham Young

University, Provo, UT 84602. Susan E. Meyer is a Research Ecologist, USDA

Forest Service, Shrub Sciences Laboratory, Provo, UT 84606.

Abstract—Cheatgrass (Bromus tectorum) individuals were genetically characterized using polymorphic microsatellite markers.

Through analysis of alleles of five polymorphic loci, genotypes

were constructed of individuals from four populations in Utah and

Nevada. There were 15 different genotypes: Whiterocks, UT, had

nine genotypes, Hobble Creek, UT, had seven genotypes, Strawberry,

UT, had four genotypes and Potosi Pass, NV, had one genotype that

was unique among all areas studied. These results are similar to

what has been found in previous germination phenology and head

smut resistance tests. Further analysis of cheatgrass populations

using these markers will assist in the analysis of cheatgrass head

smut host/pathogen dynamics and in the development of a biological

control agent for cheatgrass.

Introduction ____________________

Cheatgrass is an introduced annual grass that often

spreads into disturbed areas, rapidly establishing itself as

the dominant species. It inhibits reestablishment of native

plants (Melgoza and others 1990) and, because cheatgrass

dies early in the summer, sites with high cover of cheatgrass

are prone to frequent fires. In the arid shrubland of the Great

Basin, fires stimulated by the increase of cheatgrass heighten

mortality of important shrubs such as Artemesia tridentata

in addition to causing extensive economic damage (Young

and Evans 1978).

Through analysis of cheatgrass germination phenology,

Meyer and Allen (1999) showed that populations of cheatgrass exhibit adaptive genetic variation corresponding with

habitat. This genetic variation is presumably the result of

habitat-specific selection pressure acting on introduced

genotypes. Because cheatgrass is an obligate inbreeder,

populations are made up of an assortment of inbred lines,

each with potentially unique genotypes (Novak and others

1991). Each unique genotype may be the result of a separate

introduction of cheatgrass into a population (Novak and

others 1991). Because genetic variation in traits such as

Microsatellite Markers and Polymorphism in

Cheatgrass (Bromus tectorum L.)

Alisa P. Ramakrishnan

Craig E. Coleman

Susan E. Meyer

Daniel J. Fairbanks

germination phenology or head smut resistance exists

among the inbred lines, different lines in a population are

variously susceptible to environmental controlling factors

such as frost, drought, or disease. Meyer and others (2001)

showed that resistance of cheatgrass to Ustilago bullata

head smut is often genotype specific. This resistance polymorphism is one example of habitat-specific selection pressure. Characterization of the inbred line composition of a

population will lead to a greater understanding of the

processes leading to extensive colonization of an area by

cheatgrass.

Isozyme studies have detected some among-population

genetic polymorphism in cheatgrass, but isozyme techniques are not sensitive enough to detect inbred lines

(Novak and others 1991). Microsatellite loci (loci with dior tri-nucleotide repeats) have recently become popular in

forensics and other studies where detailed genetic information is needed (Graham and others 2000). We have

developed genetic markers using microsatellites, and they

are variable enough to detect within-population variation

in cheatgrass. Data generated from analysis of these

markers will lead to an increased understanding of the

invasion strategies of cheatgrass and may prove invaluable in developing biological control methods.

Materials and Methods ___________

We designed oligonucleotide primer sets specific to

microsatellite loci in cheatgrass by screening a cheatgrass

λ-phage genomic library with dinucleotide repeat oligonucleotide probes, sequencing positive clones, and designing primers to flank sequences with tandem repeat areas. To

construct the library, we extracted genomic DNA using a

modified CTAB protocol (Bult and others 1992). We then

digested the DNA with the restriction enzyme Sau3A and

ligated the fragments into λ-phage using the ZAP Express

Predigested Vector Kit (Stratagene: La Jolla, CA). The

ligation yielded a genomic library of approximately 100,000

clones. We screened approximately 11,200 clones for short

tandem repeats by lifting plaques onto nylon membranes

and hybridizing the recombinant DNA with poly-CA and

poly-CT oligonucleotide polymers labeled with DIG (Roche:

Indianapolis, IN). Positive clones were detected by an antibody/color detection system (NBT/BCIP) and sequenced

with a Perkin-Elmer ABI 377 automated DNA sequencer.

We detected 23 positive clones through our screening process, and 10 of the sequences generated from these clones

contained regions of six to 18 dinucleotide repeats. We
96 USDA Forest Service Proceedings RMRS-P-21. 2001

Ramakrishnan, Coleman, Meyer, and Fairbanks Microsatellite Markers and Polymorphism in Cheatgrass (Bromus tectorum L.)

designed primer sets to yield amplification products between 80bp and 300bp. We labeled one primer from each set

with a fluorescent marker for analysis on the automated

sequencer. Polymerase chain reaction (PCR) conditions were

optimized using an Eppendorf Mastercycle Gradient

thermocycler by varying temperature and magnesium

concentration.

We ran PCR reactions in 15μl or 10μl total volume with

200μM dNTPs, 1.7 to 3.3 mM MgCl2, 0.2μM each oligonucleotide of a primer pair, 0.008U/μl Taq DNA Polymerase

(Promega), and 1X PCR buffer (2mM Tris-HCl (pH 8.0),

10mM KCL, 10μM EDTA, 100μM DTT, 5 percent glycerol,

0.05 percent Tween 20, and 0.05 percent Ninidet-P40, supplied by Promega). We performed cycling regimes on a

Perkin-Elmer 9600 thermocycler with an initial 96 °C denaturing step for 3 min and a final extension step of 5 min at

72 °C. During the initial screening of the loci, we varied

optimum annealing temperatures for the primers. After the

initial screening, we switched polymerases to HotStarTaq

(Qiagen). After switching to HotStarTaq, all polymorphic

loci amplified well with an annealing temperature of 60 °C.

Polymorphic loci included Bt03, Bt05, Bt26, Bt30, and Bt33.

Results and Discussion __________

We analyzed plants from Whiterocks (cold desert, UT),

Strawberry (montane, UT), Potosi Pass (warm desert, NV),

and Hobble Creek (foothills, UT) (table 1). These areas of

study were chosen because studies by Meyer and others

(2001) focus on these areas. The first 10 plants from each

population used in our study are from the same lines used by

Meyer and Allen (1999) and Meyer and others (2001). Further research will analyze the correlation among different

studies.

In a preliminary screen of 166 individuals from these

populations, five loci were polymorphic, amplifying between

two and seven different alleles (tables 2 and 3). We are in the

process of developing more loci, and will use them to form a

more complete picture of the cheatgrass populations. This

paper offers a brief overview of the genotypes amplified by

the current loci, but is not intended to be a thorough study

of the cheatgrass populations. A complete analysis of the

populations will be made at a later date when a representative number of loci and individuals have been sampled.

Of the 50 samples from Whiterocks, we identified nine

different genotypes, with one genotype (B) representing

half of the samples (table 4). The B genotype was found in

only two of the 39 samples analyzed in Hobble Creek. The

most abundant genotypes at Hobble Creek were E and I,

both present in small numbers at Whiterocks. Five samples

from Strawberry shared a genotype present in both Hobble

Creek and Whiterocks. One Strawberry sample also shared

a genotype present only at Hobble Creek and not Whiterocks.

However, the most abundant genotype present in Strawberry was not found in either Hobble Creek or Whiterocks.

Unlike the other three collection sites, Potosi Pass shared

no genotypes with any other populations. Three of the five

loci used to construct the genotypes amplified unique

Table 1—Population habitat and location information (Meyer and others 2000).

Climate

Plant Mean annual Mean January Mean July Location

Population Elevation community type precipitation temperature temperature County State

m mm - - - - - - - - - - °C - - - - - - - - - - -

Potosi Pass 1,850 Blackbrush-juniper 250 1.7 26.5 Clark Nevada

(warm desert margin)

Whiterocks 1,450 Shadscale 180 –2.3 25.8 Tooele Utah

(cold desert)

Hobble Creek 1,800 Sagebrush-gambel oak 400 –2.1 24.8 Utah Utah

(foothills)

Strawberry 2,400 Subalpine meadow 560 –7.8 16.1 Wasatch Utah

Table 2—Summary of loci and alleles.

Locus Core repeat Size range No. of alleles Primer sequences

Bt03 (CA)7 112–114 2 Forward: GCATGTCCACCTCCATGGCCACGCC

Reverse: CTGTCTTCCTCCCTCCCTCACTTGTGTTCC

Bt05 (CT)9 165–178 8 Forward: GGGAAAGCAAGCCGTTTCCGCGTTG

Reverse: CGGTGGACGACGGGAAAGCGGAGCA

Bt26 (CT)18 152–156 2 Forward: ATCCGTCCCTCTTTCTTTGCGCTGC

Reverse: GGAGGAAGAAGAATGACCGAGAGAG

Bt30 (GT)8 112–118 4 Forward: GCCACTTTTTTTCCGAACAGACACC

Reverse: CAAAAGCAGAGTGCAGATGTAAATGAAATT

Bt33 (AG)3(AG)7(AGG)5 221–223 2 Forward: CTGCTATATCATGAGGCCATTGGGA

Reverse: AGTTTGTACAGCAGCCTGAGGCATG
USDA Forest Service Proceedings RMRS-P-21. 2001 97

Microsatellite Markers and Polymorphism in Cheatgrass (Bromus tectorum L.) Ramakrishnan, Coleman, Meyer, and Fairbanks

Table 3—Genotypes: each number

represents an allele of

Bt03, Bt05, Bt26, Bt30, and

Bt33, respectively.

Genotype ID

11111 A

12111 B

12141 C

12211 D

14111 E

14121 F

15111 G

15211 H

16111 I

12121 K

13111 L

23232 M

16121 N

17111 O

17121 P

Total 15

alleles in Potosi Pass samples. Because both genotype composition and environmental conditions among the populations vary, the most successful genotypes in each population

may be environmentally selected.

Potosi Pass is a recently invaded warm desert site with

environmental conditions different than the other populations studied. Analysis of 52 samples from Potosi Pass

showed that they were all the same genotype (M), which was

not found in any other population studied. In Meyer and

others (2001), the individuals from Potosi Pass were not

susceptible to head smut collected from any of the other

populations, but were 100 percent susceptible to head smut

from Potosi Pass. Polymorphism among populations was

also found by Meyer and Allen (1999) in their germination

studies: Potosi Pass samples exhibited different germination patterns than Whiterocks, Hobble Creek, or Strawberry. Meyer and Allen also found that Potosi Pass individuals had no vernalization requirement, whereas all other

populations require vernalization to flower (Meyer, unpublished data). The data from these previous studies and the

data presented in this paper all suggest that the Potosi Pass

population is composed of one inbred line that was introduced separately from the other lines we identified and is

unique to Potosi Pass.

If loci had mutated rapidly since the invasion of each site,

we would expect to see a completely random assortment of

alleles in each population due to mutation, with 256 possible

genotypes. However, we have only observed 15 genotypes,

indicating that observed alleles are presumably the same as

ancestral types.

References _____________________

Bult C.; Kallersjo, M.; Youngbae, S. 1992. Amplification and sequencing of 16/18S rDNA from gel-purified total plant DNA.

Plant Molecular Biology Rep. ISPMB. 10:273–284.

Graham, J.; Curran, J.; Weir, B.S. 2000. Conditional genotypic

probabilities for microsatellite loci. Genetics. 155:1973–1980.

Melgoza, G.; Novak, R.S.; Tausch, R.J. 1990. Soil water exploitation

after fires: competition between Bromus tectorum (cheatgrass)

and two native species. Oecologia. 83:7–13.

Meyer, S.E.; Allen, P.S. 1999. Ecological genetics of seed germination regulation in Bromus tectorum L. I. Phenotypic variance

among and within populations. Oecologia. 120:27–43.

Meyer, S.E.; Nelson, D.L.; Clement, S. 2001. Evidence for resistance

polymorphism in the Bromus tectorum-Ustilago bullata pathosystem: implications for biocontrol. Canadian Journal of Plant

Pathology. 23:1–9.

Novak, S.J.; Mack, R.N.; Soltis, D.E. 1991. Genetic variation in

Bromus tectorum(Poaceae): population differentiation in its North

American range. American Journal of Botany. 71:1150–1161.

Young, J.A.; Evans, R.A. 1978. Population dynamics after wildfire in

sagebrush grasslands. Journal of Range Management. 31:283–289.

Table 4—Genotypes (A-P, not J) of individuals in Whiterocks (WR), Hobble Creek (HC), Potosi Pass (PP), and Strawberry (ST).

Population Genotype

n ABCDEFGH I KLMNOP Total

WR 1 25 8 4 1 1 1 5 4 50

HC 1 2 17 2 12 1 1 3 39

PP 52 52

ST 5 1 6 13 25

Total 2 32 8 4 18 3 1 5 16 2 1 52 3 6 13 166
98 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Lyuba A. Kapustina, Botanical Institute and Botanical Garden of the

Uzbek Academy of Sciences. Current address: 4636 Laurel Ave., Glenview, IL

60026-1417.

Abstract—Geobotanic research and large-scale mapping with the

help of Geographical Information System (GIS) permit us to find out

the present state of Kyzylkum Desert shrublands, regularities of

plant communities distribution, and chemical composition of the

main dominant shrubs. Zonal vegetation types were formed on the

basis of Old Xerophilous and Old Mediterranean floras in the

Paleogene and Neogene periods. Composition of plant associations

and their anthropogenic modification largely depends on physical

and chemical properties of the soils. Climax associations of Artemisia diffusa, Astragalus villosissimus, Convolvulus hamadae, and

Ceratoides latens are connected with almost saline-free soils. Communities of Artemisia turanica, Salsola arbuscula, and S.

arbusculiformis are found on soils with the lowest salt content, and

Haloxylon aphyllum, Nanophyton erinaceum, and Salsola orientalis

communities prefer average and very saline soils. Microelement

concentration of the shrubs depends on chemical composition of

their habitats.

Introduction ____________________

The region of our investigation belongs to the Turanian

Province of the Irano-Turanian subdistrict of the SaharaGobi Desert zone (Lavrenko 1962). Mean annual temperature is +14 °C. Rainfall in the region amounts to less than

150 millimeters per year. The annual sunshine period is

about 3,000 hours.

Gypsum Desert and Saline Desert

All these types are located from 100 m to 300 m above sea

level under rather similar climatic conditions. The desert

ecosystems, by virtue of natural peculiarities, are distinguished by a rich variety of flora and fauna. There are more

than 5,000 species of vascular plants in Uzbekistan (Red

data book 1999). Among these many are rare, endemic and

relict plants, which need protection by efficient measures.

The flora of the Kyzylkum Desert contains about 937 vascular plants, and the fauna consists of over 500 species and

sub-species of vertebrates and about 950 species of nonvertebrates. The following main categories of desert ecosystems can be found in Uzbekistan: Sand Desert; Clay (or

Biodiversity, Ecology, and Microelement

Composition of Kyzylkum Desert Shrubs

(Uzbekistan)

Lyuba A. Kapustina

Gypsum) Desert and Saline Desert. All these types are

located from 100 to 300 m above sea level under similar

climatic conditions. The desert ecosystems, by virtue of

natural peculiarities, are distinguished by a rich variety of

flora and fauna.

The development of industrial enterprises and agriculture are the main reasons for changes of ecological conditions, for impoverishment of biodiversity, and for genetic

resources. Grazing has multiple effects on natural ecosystems. Animals defoliate vegetation and, consequently, affect

plant growth, vigor, reproduction, species composition, plant

cover, and biomass. At the same time animals trample the

soil thus reducing bulk density and infiltration rates and

increasing overland flow. On the other hand, as they move

around the grazing land they redistribute nutrients in the

ecosystem. All these effects, however, are minor and therefore reversible if grazing intensity is light to moderate. On

the contrary, they become severe and irreversible by heavy

grazing. Grazing intensity, therefore, is a crucial factor

affecting the Kyzylkum Desert ecosystems. Intensive pastoralism combined with overhunting has reduced wildlife and

has influenced the number and diversity of rare animal

species such as Gazella subgutturosa, Ovis polii severtzovi,

Felix margarita, Felix manul, Felix ocreata caudata, Falco

cherrug coasti, Otis undulata macqueenii, and so forth.

Material and Methods ____________

Results of long-term paleobotanical, floristic and ecological researches are used in this work (Popov 1927; Iljin 1946;

Kamelin 1979; Kapustina and others 1996). Investigation of

the present state of vegetation was carried out according to

the traditional geobotanical and GIS methods (Aleksandrova

1964; Hill and others 1996). Modifications of the vegetation

are compared with relief changes, salinization and mechanical composition of the soils. The vegetation has been classified according to Kamelin (1979). During the geobotanical

investigations in the field, ecological profiles were plotted

crossing mountain slopes and plains. Plant and soil

samples were taken along these profiles. The chemical

compositions of plants and soils were determined by

spectral analysis. Degree and type of the most saline soils

were classified according to Kovda and Egorova (Pankov

1974; Alekcandrova and Naidenov 1976).

Results and Discussion __________

Arid territories are present in Uzbekistan since the beginning of the Jurassic. Similar xerophytic flora with

representatives of Rutaceae, Capparidaceae, Geraniaceae,
USDA Forest Service Proceedings RMRS-P-21. 2001 99

Biodiversity, Ecology, and Microelement Composition of Kyzylkum Desert Shrubs (Uzbekistan) Kapustina

Frankeniaceae, and Chenopodiaceae emerged in the Southern Hemisphere in the Upper Cretaceous and Tertiary. The

formation of saline and sandy deserts began in the Paleogene. At that time savanna vegetation types were dominant.

The main savanna types were destroyed by the arctic climate

in the Pliocene. An exchange of xerophytic flora (Popov 1927;

Iljin 1946; Bobrov 1965) was distributed on the Old lands of

the Northern species between the West and East of the Old

Mediterranean region at the end of the Neogene. Many of

the Old Mediterranean genera were formed at the same time

and are the basis of the modern composition of the xerophytic

desert vegetation (Iljin 1946; Kamelin 1979). In recent times

two types, extremely arid and semiarid, of the Temperate

Floracenotype can be distinguished in the desert vegetation

of Uzbekistan (Kamelin 1979). The first group of extremely

arid types includes: Turanian Shrub-Desert type, Turanian

Psammophyton type, Irano-Turanian Psammosavanna type,

Halophyton Turanicum type and Desert Forest on humid

soils. Shrubs are a very important part of the vegetation in

the arid zone.

Types of Habitats in the Kyzylkum Desert

Gypsum Desert occupies about 29 percent of Uzbekistan

and is represented by Turanian Shrub Desert type on graybrown soils. This type was formed on the bases of Old

Mediterranean and Old Xerophilous floras in the Neogene

period. Groups of oligothermal and mesothermal euxerophilous shrubs are prevailing (Kamelin 1979). Gray-brown

soils flora consists of more than 400 species and includes

species that occur on shallow soils of residual mountains

and mixed rock; 25 percent are endemics of Middle Asia,

and 3.5 percent are endemics of the Kyzylkum Desert.

Forty one species depend on soil gypsum horizons for water

and mineral nutrition. Forty-seven species are shrubs.

Climax associations are formed by Artemisia diffusa, A.

turanica, Salsola orientalis, S. arbuscula with Carex

pachystylis and Poa bulbosa (grasses of the semisavanna

group). Xeric semishrubland on loam gray-brown soils (Artemisia diffusa communities including Artemisia turanica,

Salsola orientalis, S. arbuscula and Aellenia subaphylla)

and xeric pelitic semishrubland on clay gray-brown soils

(Artemisia turanica communities with Salsola orientalis,

S. arbuscula, Artemisia diffusa, Carex pachystylis and Poa

bulbosa) are predominant on the Southern mountain plains.

Xeric psammophytic semishrubland on sandiest gray-brown

soils (Artemisia diffusa communities with Salsola arbuscula, Ferula foetida, Calligonum leucocladum, Ceratoides

latens, Haloxylon aphyllum) and xeric shrubland on the

loam gray-brown soils (Salsola arbuscula communities

with Artemisia diffusa, A. turanica, Carex pachystylis and

Salsola orietalis) are spread on the Northern and Western

mountain plains. Artemisia diffusa and Salsola arbusculiformis communities with Artemisia terrae-albae, Rhamnus

sintenisii, Convolvulus fruticosus and Atraphaxis spinosa

are predominant on the calcareous low desert mountain

slopes. Salsola orientalis communities with Anabasis

brachiata, A. truncata, Nanophyton erinaceum and Artemisia turanica are spread on the saline soils of the mountain plains and rocks (table 1).

Formations of Anabasis salsa, A. brachiata, A. eriopoda,

A. truncata and Artrophytum lehmannianum can be considered as Old Euxerophilous Paleofloracenotype in the

Turanian desert flora, and Atraphaxis spinosa and Calligonum junceum as Old Mediterranean species emerging in the

Paleogene. At present these are spread on paleogenic slopes

of low desert mountains.

Sandy Desert is formed on sandy desert soils and loose

sands. The area of the sandy desert in Uzbekistan makes

up 27 percent of the Republic. Within the sandy desert

there are about 320 vascular plants from 31 families and 134

genera. Of these 53 percent are endemics of Middle Asia; the

rest is represented by Irano-Turanian, Turanian-Caucasian

and Turanian-European elements. Between them are 62

endemic shrubs on sandy desert soils: representatives are

Calligonum spp., Ammodendron conollyi, A. karelinii,

Salsola paletzkiana, Eremosparton flaccidum, Smirnovia

turkestana, Dendrostella arenaria, Tamarix androssovii,

Astragalus from sections, Ammodendron and Eremophysa,

Convolvulus divaricatus, C. erinaceus, Acanthophyllum

borszczowii, A. korolkovii, Ammothamnus lehmanii, and

Artemisia diffusa (Melnikova 1973). Real psammophytes

comprise 174 species; of these, 40 species are also common

in the gypsum desert and 60 in the mountain foothills. The

Table 1—Biodiversity of the shrubland in the Kyzylkum Desert.

Shrubland Area (km2)

Haloxylon persicum 58,714

H. aphyllum 6,720

Ammodendron conollyi 17,678

Salsola richteri and S. paletskiana 392

Salsola arbuscula 2,339

Low desert mountain shrubland (Rhamnus sintenisii,

Convolvulus fruticosus and Atraphaxis spinosa) 1,650

Nanophyton erinaceum 1,224

Anabasis salsa, A. eriopoda and A. brachiata 267

Astragallus villosissimus 223

Convolvulus hamadae 70

Ceratoides latens 1,064

Artemisia diffusa and A. turanica 22,229

Salsola gemmascens 22

Salsola orientalis 1,629
100 USDA Forest Service Proceedings RMRS-P-21. 2001

Kapustina Biodiversity, Ecology, and Microelement Composition of Kyzylkum Desert Shrubs (Uzbekistan)

ecological and biological peculiarities of sandy habitats

cause the occurrence of diverse forms. Trees and shrubs

form a characteristic part of the “psammophyte vegetation”

and make up to 30 percent of the flora composition. Twenty

shrub species are edificators and subedificators of plant

communities. Climax and subclimax stages are presented by

communities of the Turanian Psammophytic type that was

formed on the basis of the Old Mediterranean flora in the

Neogene. There are groups of oligothermal, and not so often

mesothermal euxerophilous psammophilous trees and

shrubs (Kamelin 1979). Salsola arbuscula, Calligonummicrocarpum, C. leucocladum, C. setosum, Haloxylon aphyllum

and Haloxylon persicum form climax and serial associations

on the sandiest gray-brown and sandy desert soils. Syngenetic stages are presented by sparse communities of

Psammodendron Irano-Turanian type on loosely fixed sandy

soils. Eroded xeric and psammophytic vegetation is wide

spread in the region of study. This type was formed from

the Old Xerophilous flora in the Paleogene and Neogene.

Later on, some communities became relict and were enriched by Turanian Psammophytic species. There are groups

of mesothermal xerophilous and psammophilous trees,

shrubs and herbs (Kamelin 1979) on eroded sandy desert

soils. In places with strong desertification on less hardened, furrowed sands and dunes as well as on sand plains

are communities of Ammodendron conollyi, Convolvulus

korolkovii, Salsola richteri, Calligonum setosum, Acanthophyllum borszczowii, and Salsola richteri. The perennials

Peganum harmala andStipagrostis pennata are dominant.

Saline Desert occupies about 3 percent of Uzbekistan. It

developed on the saltiest plains and closed depressions (such

as Mingbulak, Auminzatay, and Karakata). Characteristic

features of saline areas are constant humidity of superficial

soil horizons and occurrence of temporary reservoirs. There

are 304 species on these soil types; 30 percent of the species

are the real halophytes. Fifty two species are shrubs; some

of these form the communities of the Halophyton Turanicum

type that are widely spread on the saltiest habitats. This

type was formed on the basis of Old Xerophilous and Old

Mediterranean floras in the Paleogene and Neogene. There

are groups of mesothermal euxerophilous halophilous trees,

shrubs, perennials and rare succulent shrubs (Kamelin

1979). Haloxylon aphyllum communities with Girgensohnia

oppositiflora, Salsola praecox, Artemisia diffusa, Calligonum

erinaceum are spread on saline sandy desert soils. Salty

pelitic shrubland communities of Anabasis salsa, A. aphylla,

Halocnemum strobilaceum, Halostachys caspica, Limonium

suffruticosum, Kalidium caspicum, Frankenia bucharica,

Atriplex cana and Suaeda microphylla are spread on saline

gray-brown soils and solonchaks.

Desert Forest on humid soils covers about 3 percent of

the territory and was formed on the basis of Old Xerophilous and Arctic Tertiary Floras in the Pliocene (Kamelin

1979). The area of this type has been reduced in the

Pleistocene and Anthropogene. There are mesothermal or

rarely oligothermal hydrophilous trees and shrubs. Tamarix

ramosissima, T. elongata, T. hispida, T.laxa, T. florida,

Ulmus pumila, Populus diversifolia, Halimodendron halodendron, Lycium turcomanicum and L. ruthenicum form

communities on humid soils near the Amudaria and

Syrdarya rivers, artificial lakes and canals. Nitraria

schoberi shrub communities are a relict part of this florocenotype. The flora consists of 285 species; about 190

species are typical for these habitats only. Of these, 28

species are endemic in Middle Asia and four in Uzbekistan.

Thirty-five species are widely distributed in the river valleys of Central Asia, Dsungaria and Iran; some of them

(Populus spp., Tamarix spp. and Salix songarica) are

edificators of this vegetation.

Xerophilous Shrubs of the Semiarid Type formed the

main zonal type of the Turanian up to the Ice Age. At present

the shrub formations of this type (Artemisia juncea, Astragalus scleroxylon, Convolvulus fruticosus, Salsola

arbusculiformis, and Nanophyton erinaceun) are found only

on the paleogene slopes of the low desert mountains (such as,

Kuldzuktay, Bukantay, Tamdutay, and Kokchatay).

Ecological Types of Desert Shrubs

and Their Adaptive Strategy

Desert shrubs can be divided into three groups according

to their biological structures and ecological peculiarities

(Butnik 1991; Alimuchamedova 1979; Rachimova 1991):

hyper-xerophytes, eu-xerophytes and meso-xerophytes

(table 2).

Hyper-xerophytes have succulent assimilative organs

and are microphyllous or aphyllous. Their above ground

organs develop slowly, but root development is quick. Stability of water balance and photosynthesis, sclerotization of

axial organs and a vegetative period from spring up to late

autumn characterize this group. They have two types of

adaptive strategy. The first one, aphylly, is the strategy of

substitution and reduction of leaves by an assimilating

shoot cortex as a result of cell-division change in the growing

point. The second one, sclerophylly, consists of deep embedded stomatas, thick and complicated structure of outer

epidermis walls and fiber-cell sheath bundles to prevent

loss of water through evaporation (Butnik,1991). Transpiration rate varies from 123 to 660 mm3 of O2—fresh weight

per hour (Nigmatov and Alekseeva 1998); osmotic pressure

is 5–10 atm in spring and 44 atm in autumn. Growth occurs

in the very hot summer time, when temperatures are about

60–63 °C and have a low index of potential photosynthesis:

21–31 mg CO2/g2 per hour (Zakharianc 1971). The greater

part of the representatives of this group belong to the

Chenopodiaceae family (Haloxylon aphyllum, Halothamnus

subaphyllus, Salsola orientalis, Nanophyton erinaceum,

Anabasis eriopoda, Salsola arbuscula, S. arbusculiformis

and S. paletzkiana).

Eu-xerophytes solve the problem of evaporation decrease in the xerothermic period by dropping 70 percent of

their leaves, and have more xeromorphous than succulent

structure. Additional adaptive strategies to desert conditions without high specialization are pubescence, thickening of outer epidermis walls and sclereids (Butnik 1991).

The vegetative growth period of this group of plants continues from spring to late autumn. Intensity of transpiration

varies from 1,170 mm3 of O2 of fresh weight per hour (spring)

up to 180 (summer); osmotic pressure is 6–9 atmospheres

in spring and 67 in summer (Rachimova 1991); index of

potential photosynthesis is higher than in the first group
USDA Forest Service Proceedings RMRS-P-21. 2001 101

Biodiversity, Ecology, and Microelement Composition of Kyzylkum Desert Shrubs (Uzbekistan) Kapustina

–31 to 50 mg CO2/g2 per hour. Eu-xerophytes can stand

+59 °C; their root systems go 4 to 5 m deep. Desert shrubs

Ceratoides latens, Ammodendron conollyi, Astragalus villosissimus, and Kochia prostrata belong to this group.

Meso-xerophytes drop 80 to 100 percent of their leaves in

the hottest period of summer. They are not as adapted to the

xerothermic period like hyper-xerophytes and eu-xerophytes

and have some elements of xeric structure: thin leaves,

covered with hairs, biological repose in summer time and the

possibility to use essential oils in the hot time for protecting

the plant from excessive heating due to very high temperatures. Artemisia shrubs of the subgenus Seriphidium belong

to this group. Species of this subgenus have three vegetative

phases: first is mesothermic (in the spring)—for growing and

development, second is xerothermic (in the summer) for

biological rest, and third is microthermic (in the autumn and

winter) for seed production and dying of the inflorescences.

The root system of these shrubs goes about 2 to 2.5 m deep.

Intensity of transpiration of this group varies from 1,704 to a

maximum of 2,388 mm3

 O2 for 1 g of fresh weight per hour

(spring) up to 30–80 (summer) and 410 (autumn); osmotic

pressure is 12 atm in spring time, 28 in summer and 32 in

autumn; index of potential photosynthesis is 44 to 55 mg CO2/

g2

 per hour (Rachimova 1991).

Adaptation to Saline Soils

The distribution of vegetation in the Uzbekistan Desert

zone depends on the adaptation to the moist saline soils.

Analysis of the desert shrub communities distribution and

chemical composition of soils have shown that three

edaphotypes (Bikov 1981; Freitag 1991; Akjigitova 1996)

can be distinguished in the Kyzylkum Desert: euhalophytes,

hemihalophytes and halo-glycophytes.

Euhalophytes have a wide tolerance range and are very

well adapted to the average and high saline soils containing

magnesium-calcium sulphate. Dry residue of the complete

water extract from these soils is about 1.8 to 2.5 percent

(table 3). Due to their adaptation they belong to salt accumulating- and salt-excreting halophytes. Haloxylon aphyllum,

Table 2—Ecological types of desert shrubs.

Intensity of

transpiration (mm3 of Osmotic Index of potential

Type of Adaptive 02 for the gram of pressure photosynthesis Vegetative

desert shrubs Species strategy fresh weight per hour) (atm) (mg CO2/g2 per hour) growth period

Hyper-xerophytes Haloxylon aphyllum, Aphylly and 123–660 5–44 21–31 From spring

Halothamnus subaphyllus, sclerophylly up to late autumn

Salsola orientalis,

Nanophyton erinaceum

and Anabasis eriopoda,

Salsola arbuscula,

S. arbusculiformis and

S. paletzkiana

Eu-xerophytes Ceratoides latens, Defoliation 1,170–180 16–9–67 31–50 From spring time

Ammodendron conollyi, (70 percent), to late autumn

Astragalus villosissimus pubescence,

and Kochia prostrata thicknening of

epidermis walls

Meso–xerophytes Artemisia diffusa, Defoliation 1,704–30 12–32 44–55 Three vegetative

A. turanica and (100 percent), (80)–410 phases

A. ferganensis thin leaves,

pubescence,

biological rest

in summer time

Table 3—Chemical composition of soils in the zone of maximum root distribution of dominant shrubs (percent).

Species Dry residue HCO3 Cl SO4 NO3 Ca Mg K Na

Haloxylon aphyllum 2.58 0.6 2.45 32.9 0.16 27.4 1.6 0.08 6.81

Salsola orientalis 2.39 0.6 2.4 32.1 0.65 29.0 3.3 0.08 3.45

Salsola arbusculiformis 0.37 0.6 0.1 4.46 0.02 4.2 0.75 0.36 0.16

Salsola arbuscula 0.1 0.9 0.1 0.6 0.03 0.5 0.2 0.2 0.73

Artemisia diffusa 0.08 0.8 0.1 0.5 0.03 0.5 0.55 0.18 0.13

Artemisia turanica 0.13 0.8 0.05 1.1 0.03 1.25 0.2 0.34 0.19
102 USDA Forest Service Proceedings RMRS-P-21. 2001

Kapustina Biodiversity, Ecology, and Microelement Composition of Kyzylkum Desert Shrubs (Uzbekistan)

Salsola orientalis, S. gemmascens, Anabasis salsa, A. brachiata and Nanophyton erinaceum are Chenopodiace shrubs

and they are predominant in this group.

Hemihalophytes are shrubs of average saline soils containing magnesium-calcium sulphate. Dry residum of the

complete water extract from these soils varies from 0.9 to

1.7 percent (table 3). Species of this group are Salsola

arbuscula, Arthrophytum lehmannianum, Nitraria schoberi, Artemisia turanica, A. ferganensis, and A. santolina;

they are sometimes spread on lower or high saline soils,

too, but do not form communities in this habitat.

Haloglycophytes are shrubs with weak tolerance to

very saline soils. Dry residue of the complete water extract

from these soils is not more than 0.3 percent (table 3).

Artemisia diffusa, Astragalus villosissimus, Convolvulus

hamadae, S. arbusculiformis and Ceratoides latens belong

to this group. Sometimes communities of these species are

found on almost saline-free soils (the dry residue of the complete water extract from these soils is about 0.08 percent).

The chemical composition of plants growing in the same

habitats, but belonging to different life-forms, is various and

depends on physiological and ecological factors (Biogeochemical and Geobotanical Investigations 1972). According

to chemical composition of desert shrubs in the Kyzylkum

Desert we could establish that the following species accumulate elements most actively: Artemisia diffusa and A.

turanica—Cu, W, V, Cr, Pb, Zn, Ni, Mo, Co, Bi,P and Sn;

Artemisia sogdiana—U, Pb, Cd, Zn and Mo; Astragalus

villosissimus—Ni, Ag, Pb, Sr, Zn, P and Cu; Salsola

arbuscula—Mn, Sr, Ba, Pb, U and Ni; Salsola orientalis—

Sr, Ba; Calligonum microcarpum—P, Pb and Ni; Ceratoides

latens—Mo, Zn, Cu; and Nanophyton erinaceun—Ag,Cu and

Pb (fig. 1). Pb was best accumulated Artemisia diffusa and

Calligonum microcarpum; Zn and Cu—Artemisia diffusa

and Halocnemum strobilaceum; V and Cr—Artemisia diffusa.

Conclusion_____________________

Shrublands are predominant in the Kyzylkumm

Desert.Three ecological types of desert shrubs widely spread

on different soils. The greater part of the representatives of

hyper-xerophytes are adapted to average and very saline

soils and belong to euhalophytes. Chemical compositions of

desert shrubs (Artemisia diffusa, Calligonum microcarpum,

Ceratoides latens and Salsola arbuscula) can be used us

indicators of the polluted zones and deposits.

10

9

8

7

6

5

4

3

2

1

0

4

3.5

3

2.5

2

1.5

1

0.5

0

3

2.5

2

1.5

1

0.5

0

0.070

0.060

0.050

0.040

0.030

0.020

0.010

0.000

Cu concentration in the plants

Zn concentration in the plants

Pb concentration in the plants Ag concentration in the plants

Row 5

Plant species

Row 4

Plant species

Row 6

Plant species

Row 7

Plant species

1 2 3 4 5 6 7 8 9 10 11 12

1 2 3 4 5 6 7 8 9 10 11 12 1 2 3 456 789 10 11 12

1 2 3 4 5 6 7 8 9 10 11 12

Concentration Concentration

Concentration

Concentration

1. Calligonum microcarpum 7. Artemisia diffusa

2. Salsola arbuscula 8. Nanophyton erinaceum

3. Astragalus villosissimus 9. Ceratoides larens

4. Aellenia subaphylla 10. Anabasis salsa

5. Haloxylon aphyllum 11. Kochia prostrata

6. Salsola orientalis 12. Halocnemum strobilaceum

Figure 1—Microelement composition of shrubs in the Kyzylkum Desert (percent concentration: n x 0.001).
USDA Forest Service Proceedings RMRS-P-21. 2001 103

Biodiversity, Ecology, and Microelement Composition of Kyzylkum Desert Shrubs (Uzbekistan) Kapustina

References _____________________

Aleksandrova, V.; 1964.Study of vegetation cover changes.In Field

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Alimuchamedova S., 1983. Anatomy. In book: Adaptation of the

forage plants to conditions of arid zone in Uzbekistan: 173–178,

192–194, 209–211.

Akjigitova, 1996. Halophyllous Vegetation of Middle Asia.Plant

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i geobotanicheskie issledovania),1972. Leningrad. 280 p.

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Berlin-Stuttgart: 281–292.

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Associations at the Bukan-Getimtaus System of Ostans Mountains. Plant Life in Southwest and Central Asia, Turkish: 573–579.

Lavrenko, E. M.1962. Osnovnii cherti botanicheskoi geographii

pustin Evroasii i Severnoi Afriki. Moskva-Leningrad. 169 p.

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Nigmatov, M. M. and Alekseeva, L. N. 1998.Phisiologo-biochemical

investigations in Kyzylkum Desert Plants. Journal of Arid Land

Studies, v.7: 205–209.

Rachimova T.1991.Nauchnii osnovi sozdania bogarnih

kuliturphitosenozov pri optimizatii degradirovannih i

narushennich zemel. In book:Aktualinii problemi kompleksnogo

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In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Lyubov A. Kapustina,Botanical Garden and Botanical Institute, Academy

of Sciences of the Republic of Uzbekistan, 32, F. Khodzhaev str. Tashkent

700143, Uzbekistan. Current address: 4636 Laurel Ave., Glenview, IL 60026-

1417. Montserrat Torrell and Joan Vallès, Laboratori de Botànica, Facultat

de Farmàcia, Universitat de Barcelona, Av. Joan XXIII, s/n, 08028 Barcelona,

Catalonia, Spain.

Artemisia Communities in Arid Zones

of Uzbekistan (Central Asia)

Lyubov A. Kapustina

Montserrat Torrell

Joan Vallès

Abstract—Central Asia, and particularly the former Soviet Middle

Asian countries, with more than 180 taxa (45 endemics), is one of the

centers of origin and speciation of the genus ArtemisiaL.(Asteraceae,

Anthemideae). Several species of this genus, mainly belonging to

subgenus Seriphidium (Besser) Rouy, are shrubs that dominate the

landscape and form large communities in arid (desertic, semidesertic,

steppic, and other) zones of this region. Arid lands constitute

approximately 90 percent of the territory of Uzbekistan, and there

are approximately 40 Artemisia species. In this paper we present a

characterization of some of these species (including six Central

Asian endemics) and communities, with ecological, chorological

(with a distribution map), biogeographical, cytogenetic, and chemical data. We also include some references to plant use and management in these areas.

Introduction ____________________

The region of our investigation belongs to the Turanian (or

Aralo-Caspian) and Turkestanian Provinces of the IranoTuranian region in the Tethyan (Ancient Mediterranean)

floristic subkingdom (Takhtajan 1986). The Middle Asiatic

Desert includes the Irano-Turanian Desert region that occupies the southern portion of the Aralo-Caspian Desert and

the southern part of Kazakhstan, including Dsungaria. The

Central Asiatic Desert comprises a part of Dsungaria, the

Gobi Desert, the western part of Ordos on the great bend of

the Hwan-Ho, Ala-Schan, Bei-Schan, and the Tarim basin

(Kaschgaria), together with the Takla-Makan Desert and

the more elevated Tsaidan basin (Walter 1979).

One hundred and eighty Artemisia species are present in

Middle Asia, 45 of which are endemic to this zone (Poljakov

1961b). From these taxa, 36 grow in Uzbekistan, some of

them in desert or semidesert zones, and others in mountain

zones. The existence of 19 Middle Asian endemic species of

the genus (Vvedenskii 1962) is remarkable in Uzbekistan.

Investigations of the Artemisia species and their distribution were carried out using basic ecogeographical and

mapping methods. In addition to the location of Artemisia

species and communities in Uzbekistan (fig. 1), we present

some data on general distribution, ecology, chemical composition, chromosome numbers, and uses of the main taxa of

the genus (table 1).

The species belonging to the subgenus Seriphidium, which

includes most of the Central Asian taxa of Artemisia that are

relevant in the landscape, have some elements of xeric

structure: tomentose leaves, biological repose in summer,

and the possibility to expel essential oils in hot weather for

plant protection from excessive heating due to very high

temperatures. Species of this subgenus have three vegetation phases: (1) mesothermic (in spring) for growing and

development, (2) xerothermic (in summer) for biological

repose, and (3) microthermic (in autumn and winter) for

seed production and death of the inflorescences. The structure of A. ferganensis, A. porrecta, and A. serotina is simpler,

because they have only a very small woody perennial stem

(Mailun 1976). Most of the species in this subgenus are

predominant in vegetation and good forage plants for livestock. Dry mass content of the forage plants of desert

shrubland with predominating Artemisia species varies

from 1.3 to 2.6 centner per hectare. Forage plant dry mass

protein content varies from 0.15 to 0.09 centner per hectare.

Some species are used for other purposes, such as A. juncea

(medicine and perfumery) and A. serotina (soap-boiling)

(Larin 1937; Goryaev and others 1962).

Essential oil content of Artemisia species predominating

in vegetation in different zones of Uzbekistan varies from

0.32 to 3.1 percent, the highest concentrators being A. dracunculus (up to 3.1 percent), A. ferganensis (up to 2.1 percent), and

A. porrecta (up to 1.5 percent) (Goryaev and others 1962).

Camphor is present in the essential oils of A. leucodes (93

percent), A. ferganensis (85 percent), and A. porrecta

(37 percent); cinneol in A. serotina (78 percent), A. porrecta

(47 percent), and A. leucodes (35 percent); and thujone in

A. baldshuanica (60 percent) (Goryaev and others 1962).

Flavonoids are present in A. leucodes, A. dracunculus, and

A. serotina; sesquiterpene lactones in A. tenuisecta, A. santolina, A. serotina, A. juncea, and A. leucodes; coumarins in

A. porrecta, A. diffusa, and A. dracunculus; acetylenes in

A. turanica and A. dracunculus (Marco and Barberá 1990).

Essential oil concentration in weed species varies from

0.34 percent (A. tournefortiana and A. annua) to 1 percent

(A. vulgaris, A. scoparia, and A. absinthium—up to 2 percent) (Goryaev and others 1962). Most of these weed species

also contain acetylenes, coumarins, flavonoids and sesquiterpene lactones (Marco and Barberá 1990).
USDA Forest Service Proceedings RMRS-P-21. 2001 105

Artemisia Communities in Arid Zones of Uzbekistan (Central Asia) Kapustina, Torrell, and Vallès Figure 1—Distribution of the most widespread Artemisia in Uzbekistan: communities dominated by Artemisia species (1–14) and weed taxa of this genus (15–21). 10. Artemisia baldshuanica with Carex pachystylis, Amygdalus bucharica, Otostegia bucharica, and Pistacia vera on dark serozem soils. 11. Artemisia lehmanniana with Festuca sulcata on light-brown soils. 12. Artemisia dracunculuswith Cousinia allolepis, C. macilenta, Acanthophyllum alatavicum, Festuca sulcata, and Prangos pabularia on light-brown soils. 13. Artemisia porrecta with Carex pachystylis, Salsola sclerantha, Phlomis thapsoides, and Eremostachys eriocalyx on serozem soils, sometimes slightly salty.

● 14. Artemisia persica with Cerasus verrucosa, Dactylus glomerata, Poa nemoralis, Agropyron trichophorum, and Origanum tyttanthum on chernozem soils.

15. Artemisia sieversiana.

16. Artemisia scoparia.

17. Artemisia tournefortiana.

18. Artemisia annua.

n 19. Artemisia absinthium.

20. Artemisia vulgaris.

▲ 21. Artemisia serotina.

1. Artemisia terrae-albae with Anabasis salsa, Salsola orientalis, and Haloxylon ammodendron on

gypsum gray-brown soils.

1 A. Artemisia terrae-albae with Haloxylon persicum, Calligonum setosum, and Carex physodes on

sandy desert soils.

2. Artemisia diffusa with Calligonum leucocladum, Astragalus villosissimus, and Carex physodes

on sandy desert and sandy gray-brown soils.

2A. Artemisia diffusa with Salsola orientalis, Carex pachystylis, Salsola arbuscula, and Ferula foetida

on gray- brown soils.

✩ 3. Artemisia turanica with A. diffusa, Carex pachystylis, Poa bulbosa, Salsola arbuscula, and

S. orientalis on gray-brown soils.

4. Artemisia santolina with Carex physodes and Mausolea eriocarpa on sandy desert soils.

5. Artemisia junceawith A. diffusa, Ceratoides latens, Convolvulus fruticosus, Astragalus scleroxylon,

Zygophyllum atriplicoides, and Salsola arbusculiformis on gray-brown soils of the low mountain

slopes.

6. Artemisia ferganensis with A. diffusa, Halocharis hispida, and Climacoptera longistylosa, on

saltiest light serozem soils.

7. Artemisia leucodes with A. diffusa, Convolvulus hamadae, and Astragalus villosissimus.

8. Artemisia sogdiana with Carex pachystylis, Poa bulbosa, Bromus danthoniae, Ceratocarpus

utriculosus, and Vulpia myuros on typical serozem soils.

9. Artemisia tenuisecta with Elytrigia trichophora, Prangos pabularia, Inula grandis, and Amygdalus

spinosissima on typical and dark serozem soils.

9A. Artemisia tenuisecta with Juniperus seravschanica, J. semiglobosa, and Elytrigia trichophora on

typical brown soils.
106 USDA Forest Service Proceedings RMRS-P-21. 2001

Kapustina, Torrell, and Vallès Artemisia Communities in Arid Zones of Uzbekistan (Central Asia) Table 1—Systematic, chorological, ecological, chemical, and karyological data on Uzbek Artemisia species, and main uses of these taxa (information drawn from references and our personal knowledge). Species Chromosome Subgenus (and life form) Distribution area Ecology Chemical composition Utilization number (2n) Artemisia A. vulgaris L. Central Asia, Siberia Weed species, from plain Essential oil containing cinneol, thujone, Food for livestock, 16 (perennial) China, Afghanistan, up to the middle zone of paraffin, and borneol. Acetylenes, rabbit, beaver, gopher, Japan, India, Caucasus, mountains, river beaches, coumarins, flavonoids, and sesquiterpene marmot. Used for North America, gardens, and meadows lactones. Root contains inulin, tannic medical purposes by Mediterranean region, substances, and resin. Leaves contain local people. Leaves and Mongolia, West Europe, vitamins A and C. stems are used as a European part of the condiment for meat dishes. former Soviet Union A. persica Boiss. Central Asia (Tian-Shan, Road metal slopes from foot Essential oil containing pinene, Mountain specimens of 18 (perennial) Pamir-Alai), Iran, Tibet, up to middle zones of the camphorene, camphor, borneol, and this species can be used Afghanistan mountains bornilacetate. Leaves and steams contain to obtain camphor. alkaloids, acetylenes, and coumarins. A. tournefortiana Central Asia, Caucasus, River valleys from plain Essential oil containing aldehydes, 18 Reichenb. (annual Tibet, Afghanistan, Iran up to the middle zone of phenols, alkaloids, acetylenes, and or biennial) mountains, forests near sesquiterpene lactones. rivers, and weed species in gardens A. annua L. Central Asia, Siberia, Weed, ruderal in gardens, Essential oil containing pinene, Perfumery. Condiment. 18 (annual) Europe, Iran, China, fields, villages, and towns camphene, cinneol, artemisiactene, Root extract used for Afghanistan, Japan, and artemisiactane. Alkaloids, wool and leather dyeing North India, North Africa, acetylenes, coumarins, flavonoids, in lemon-yellow color. North America, Far East, and sesquiterpene lactones. Caucasus Absinthium A. absinthium L. Central Asia, Siberia, From plain up to the middle Essential oil containing absinthol, Food for rabbits. 18 (perennial) Western Europe, Iran, zone of mountains, river thuyone, felandrene, pinene, cadinene, Essential oil is used for Afghanistan, North India, beaches, forests near rivers terpenes, and absinthin. Acetylenes, pharmaceutical and North America, Caucasus, coumarins, flavonoids, and sesquiterpene vodka industries. Leaves Mediterranean, European lactones. Leaves contain vitamin C and are used as spice. Plant part of former Soviet Union carotene. is used for medical purposes from ancient time. A. sieversiana Central Asia, Siberia, Road metal slopes from Essential oil. Alkaloids in leaves, stems, This plant can be used for 18 Willd. (annual or China, Japan, Mongolia, foot up to middle zones of and flowers. Acetylenes, coumarins, siloing. biennial) east of the European part mountains, river and canal flavonoids, and sesquiterpene lactones. of former Soviet Union beaches, weed species in gardens and fields Dracunculus A. scoparia Central Asia, Siberia, Weed species widely spread Essential oil containing 

α- and β-pinene, Food for camel, horse, 16

Waldst. et Kit. Western Europe, on plains, foothills, and and myrcene. Acetylenes, coumarins, sheep, and rabbit.

(annual or China, Afghanistan, gardens flavonoids.

biennial) Japan, North India,

Caucasus, European part

of former Soviet Union (con.)
USDA Forest Service Proceedings RMRS-P-21. 2001 107

Artemisia Communities in Arid Zones of Uzbekistan (Central Asia) Kapustina, Torrell, and Vallès Table 1—Con. Species Chromosome Subgenus (and life form) Distribution area Ecology Chemical composition Utilization number (2n) (con.) A. dracunculus L. Central Asia, Siberia, Subalpine and alpine Essential oil containing sabinene Perfumery, used by local 18, 36, (perennial) south of the European meadows from 2,800 to and myrcene. people. Food plant. 72, 90 part of former Soviet 3,700 m on fulvous type Union, Minor Asia soils Afghanistan, North America, Mongolia Seriphidium A. tenuisecta Central Asia Communities widespread on Essential oil. Alkaloids, organic acids, Food for livestock. 18 Nevski the slopes of the lower and and ethers. Sesquiterpene lactones. (perennial) middle zones of Tian-Shan and Pamir-Alai Mountains Section A. ferganensis Central Asia Communities on loam, Essential oil containing camphor, Food for livestock. 36 Seriphidium Krasch. ex Poljak. loam-road metal and sandy

α-thujone, carvone, cinneol.

(perennial) loam salty soils of river Sesquiterpene alcohols. Green

valleys, from foothills up to shoots and leaves contain alkaloids.

middle mountain zones

A. porrecta Central Asia On loam, road metal and Essential oil containing camphor, Food for livestock. 18

Krasch. ex Poljak. stony slopes from foothills cinneol, aldehydes, phenols, and

(perennial) up to middle mountain zones azulene sesquiterpenes. Coumarins.

A. serotina Bunge Central Asia On the loam and loam-road Essential oil containing cinneol, Food for livestock. Used 18

(perennial) metal, sometimes slightly camphor, acids, and carotene. for soap-boiling.

salty soils of plains, foothills, Stem and leaves contain alkaloids

and lower zones of the and flavonoids.

mountains

A. turanica Central Asia, Iran, Sandy, loam, gray-brown Essential oil. Tannin. Resin. Acetylenes. Food for livestock. 18

Krasch. Afghanistan and gray-brown road metal

(perennial) soils of the desert plains

and foothills

A. diffusa Krasch. Central Asia Sandy and gray-brown Essential oil. Coumarins. Food for livestock. Used 36

ex Poljak. desert soils, serozem to make hay stocks by

(perennial) of the foothills local people.

A. sogdiana Central Asia, Afghanistan Loam-road metal soils Essential oil. 36

Bunge (perennial) (sometimes slightly salty)

and stony slopes from foothills

up to middle mountain zones

A. baldshuanica Central Asia (South Loam-road metal and stony Essential oil containing 

α- and β-thujone, 36

Krasch. et Zapr. Pamir-Alai) slopes of the North thujone alcohol, isothujvalerianate, and

(perennial) Exposition from foothills up aldehydes.

to middle mountain zones

A. lehmanniana Central Asia Subalpine and alpine Essential oils. Phenols, cetones, Unknown

Bunge (perennial) meadows from 2,800 to sesquiterpenes.

3,700 m on fulvous type soils
108 USDA Forest Service Proceedings RMRS-P-21. 2001

Kapustina, Torrell, and Vallès Artemisia Communities in Arid Zones of Uzbekistan (Central Asia)

Artemisia Communities

in Uzbekistan ___________________

The Uzbek Desert zone is included in the Turanian Province. The mean annual temperature is 14 °C, and the mean

annual precipitation is 130 mm per year. The annual duration of the sun radiance is about 3,000 hours. Climax communities of the Turanian Desert type are dominated by

A. diffusa Krasch., A. turanica Krasch., and A. terrae-albae

Krasch. Figure 1 shows the distribution of the most widespread Artemisia species in Uzbekistan, not only those that

are dominating in different communities, but the weed taxa

of the genus as well.

Artemisia diffusa (fig. 2A) is a South Turanian species

endemic of Middle Asia. It is a very ramified shrub, about 20

to 50 cm tall, with dense white indumentum. This plant is

more widespread and predominant in different soil types of

the desert zone in Uzbekistan. About 50 A. diffusa associations have been described in Uzbekistan, which contain 140

vascular plant species: 34 shrubs, 28 perennial herbs, and 77

annual species (Granitov 1964; Melnikova 1973; Momotov

1973; Zakirov 1973).

Artemisia turanica (fig. 2A) is distributed in Middle Asia,

Iran, and Afghanistan (Vvedenskii 1962). It is a shrub about

20 to 40 cm tall, with violet-brown (or black) stems. It is often

codominant in the A. diffusa communities and sometimes

predominante in salty loam gray-brown soils of the premountain plains. Desert Artemisia (A. diffusa, A. turanica)

are very polymorphic, and in their communities there are

often plants that have been considered by several authors as

hybrids between both species, even though they are closer to

A. turanica in habit (Poljakov 1958, 1961a; Momotov 1973).

Anatomical characteristics of those species are variable in

the different types of the soils of Kyzylkum Desert. In the

drier conditions of loam soils, leaves are flatter, with denser

nervation; water-carrier facing cells are larger and thickwalled mesophylle; sprouts are more lignified. Artemisia

turanica is more adapted to strict conditions and has a

higher stomata density than A. diffusa (Alimuchamedova

1983; Padunina and Momotov 1983). Twenty A. turanica

associations were described in Uzbekistan. Floral composition varies from 25 to 57 (5 shrubs, 16 perennial herbs, and

36 annual) species (Granitov 1964; Melnikova 1973; Momotov

1973; Zakirov 1973). Xeric pelitic shrubland of A.diffusa and

A. turanica communities withSalsola orientalis, S. arbuscula,

Carex pahystylis, and Poa bulbosa predominate on loam and

clay gray-brown soils of the mountain plains. Xeric

psammophytic communities of A. diffusa with Calligonum

leucocladum, Astragalus villosissimus, Carex physodes,

Convolvulus hamadae,Salsola arbuscula, and Ferula foetida

predominate on sandy gray-brown soils and sandy desert

soils. Xeric petrophytic shrubland of A. diffusa and A.

turanica with Salsola arbusculiformis, Convolvulus

fruticosus, Stipa aktauensi, Astragalus scleroxylon, and

Atrophaxis spinosa is spread on the calcareous slopes of low

desert mountains. Salty shrubland of these species with

Climacoptera lanata, Gamanthus gamocarpus, and Girgensohnia oppositiflora is distributed on saline gray-brown soils

and solonchaks.

Artemisia terrae-albae (fig. 2B), a North Turanian species,

is one of the most important plants in the plant cover of

Table 1—Con.

Species Chromosome

Subgenus (and life form) Distribution area Ecology Chemical composition Utilization number (2n)

A. santolina Schrenk. Central Asia, Iran, China Sandy, sometimes slightly Sesquiterpene lactones. Food for livestock. 18

(perennial) salty, desert soils

A. terrae-albae Central Asia, Mongolia, Gypsum gray-brown soil of Essential oil containing cuminaldehyde, Food for livestock. Unknown

Krasch. (perennial) Western China plateau and sandy desert cinneol, borneol, camphor, and

soils, northern part of the artemisiacetone.

desert zone

Section A. juncea Kar. et Central Asia, China Alluvial road metal-sandy- Essential oil. Tannic substances. Resin. 18

Junceum Kir. (perennial) loam soils of the plain, Sesquiterpene lactones.

loam-road metal and stony

slopes from foothills up to

lower mountain zones

A. leucodes Central Asia Sandy desert soils of the Essential oil containing camphor, cinneol, Used for medicinal 18

Schrenk. (annual plains, loam and road metal- cis-pinocampheol, borneol ether, purposes and perfumery.

or biennial) loam soils of the foothills isovalerianic acid, azulene sesquiterpenes,

and lower mountains and azulenes. Santonin. Flavonoids and

sesquiterpene lactones.
USDA Forest Service Proceedings RMRS-P-21. 2001 109

Artemisia Communities in Arid Zones of Uzbekistan (Central Asia) Kapustina, Torrell, and Vallès

Figure 2—Communities dominated by different Artemisia species in Uzbekistan. (A) A. diffusa

and A. turanica. (B) A. terrae-albae. (C) A. santolina. (D) Mausolea eriocarpa (Artemisia

eriocarpa). (E) A. sogdiana. (F) A. serotina. (G) A. ferganensis. (H) A.baldshuanica.
110 USDA Forest Service Proceedings RMRS-P-21. 2001

Kapustina, Torrell, and Vallès Artemisia Communities in Arid Zones of Uzbekistan (Central Asia)

Kazakhstan and the Central Asian Desert zone (Musaev

1968; Safronona 1998), including the Uzbekistan Northern

Desert part. It is a shrub about 25 cm tall. The leaves have

an epidermis of small cells with a thick cuticle layer and are

densely tomentose (Zakrzevski and Korovin 1935). Epidermic cells contain tannic substances. The distribution area of

this species includes Middle Asia and Mongolia (Vvedenskii

1962). Artemisia terrae-albae communities (with Anabasis

salsa, Salsola orientalis, and Haloxylon ammodendron) are

widespread on gypsum gray-brown soils of the Usturt Plateau, and occur in a small territory (with Haloxylon persicum,

Calligonum setosum, and Carex physodes) in the desert

sandy soils, and sandy gray-brown soils in the North Desert

zone. There are 10 A. terrae-albaeassociations in Uzbekistan.

Their floral composition varies from seven species on gypsum soils to 48 species (22 percent shrubs, 27 percent

perennial herbs, and 51 percent annuals) on sandy graybrown soils (Momotov 1973).

Artemisia santolina (fig. 2C) is a desert white tomentose

shrub about 40 to 60 cm tall. This species spreads in Middle

Asia, Iran, and China, but very seldom predominates in the

vegetation cover of Uzbekistan. Small spots of A. santolina

communities with Mausolea eriocarpa (Artemisia eriocarpa)

(fig. 2D) and Carex physodes occur in sandy desert soils of the

southwest part of the desert zone near the Amu-Daria River.

Their floral composition is about 12 species.

Shrublands with A. sogdiana, A. serotina, A. ferganensis,

A. porrecta, A. baldshuanica, and A. tenuisecta communities

predominate in the semidesert and low mountain zones of

Uzbekistan (Mailun 1976). Soils are represented by serozems

with gypsum or detritus in some places. Average annual

temperature is 12 to 15 °C. Average annual precipitation is

250 to 400 mm. The width of the mountain semidesert belt

is 30 to 50 km and makes up two-thirds (more than 64,000

km2

) of the mountain territories of the Republic.

Artemisia sogdiana (fig. 2E) is a shrub about 40 cm tall,

with 10 to 15 cm that is woody perennial part. Leaves are

slightly tomentose. The epidermis is thicker than that of

other Artemisia species. Artemisia sogdiana stomata size

and distribution are similar to those of A. turanica. Epidermal cell walls have a winding structure. These are mesomorphic indications (Alimuchamedova 1983). Distribution area

of A. sogdiana expands in Middle Asia and Afghanistan

(Vvedenskii 1962). Communities are widespread from

premountain plains up to low mountain zones (500 to 800 m).

There are 28 A. sogdiana associations in Uzbekistan. Their

floristic composition is approximately 150 species (Mailun

1976). Most typical species in A. sogdiana communities are

Carex pachystylis, Poa bulbosa,Bromus danthoniae, Ceratocarpus utriculosus, Vulpia myuros, Cousinia resinosa, Phlomis

thapsoides, Eremostachys eriocalyx, and Psoralea drupacea.

Artemisia serotina (fig. 2F), endemic to Middle Asia, has a

short perennial part and numerous herbaceous stems about

40 to 80 cm tall, very tomentose in the beginning of the

vegetation period and almost glabrous to the end. This plant

grows on different types of soils from plains to lower parts of

mountain zones (Vvedenskii 1962) and is very often codominant in A. sogdiana and A. serotina communities, with

Phlomis thapsoides, Cousinia resinosa, Haplophyllum

perforatum, Solenanthus turkestanicus, Poa bulbosa, Carex

pachystylis, Garhadiolus angulosus, Lens orientalis, and

Medicago rigidula. These communities are secondary and

occupy very small places in Uzbekistan.

Artemisia ferganensis (fig. 2G) is an endemic shrub to

Central Asia, with its perennial part about 10 cm and only

a few tomentose offshoots about 60 to 100 cm tall. This plant

grows in different type of soils and sometimes on very salty

places like a halophyte. According to anatomical and morphological indications, A. ferganensis has less xeromorphic

structure (bigger leaves, stomata, and main rib; dense leaf

nervation) than A. turanica, A. diffusa, and A. sogdiana

(Alimuchamedova 1983). Communities dominated by Artemisia ferganensis, with Camphorosma monspeliaca, Salsola

orientalis, Kalidium caspicum, Climacoptera intricata,

C. longistylosa, Suaeda arcuata, and Halocharis hispida,

occupy small salty places near Aidar Lake and in the Fergana

Valley. Sometimes A. ferganensis predominates on loam

soils of the low mountains with Taeniatherum crinitum,

Aegilops truncialis, Bromus danthoniae, Poa bulbosa, Hordeum bulbosum, Phleum paniculatum, Alyssum marginatum, Srigosella trichocarpa, Psoralea drupacea, and Eremurus sogdianus. Artemsiia ferganensishas been planted in

the Aral Sea region for arid land regeneration and pastureimproving purposes.

Artemisia porrecta is an endemic shrub to Middle Asia,

with erect herbaceous stems about 75 cm tall. Its morphological structure is very close to that of A. ferganensis, but

they differ by inflorescence form. There are three associations of A. porrecta, with Carex pachystylis, Phlomis

thapsoides, Eremostachys eriocalyx, Salsola sclerantha,

Girgensohia oppositiflora, Hordeum leporinum, and Aegilops

squarrosa on salty soils along the rivers from lower to middle

mountain zones in Uzbekistan (Mailun 1976).

Artemisia baldshuanica (fig. 2H) is an endemic species to

Middle Asia, with a very limited distribution area in the

South Pamir-Alai Mountain system. This shrub has erect

stems about 60 to 100 cm tall with a woody part 20 to 40 cm

(Vvedenskii 1962). Artemisia baldshuanica communities

are spread on northern slopes, sometimes with crushed

stones, from foothills up to the middle part of the mountains.

There are three associations with this species in Uzbekistan,

with Dactylis glomerata, Agropyron trichophorum, Calamagrostis epigeios, Origanum tyttanthum, Phlomis bucharica,

Ziziphora brevicalyx, Muretia fragrantissima, Agropyron

trichophorum, Carex pachystylis, Poa bulbosa, Gentiana

olivieri, Gagea stipitata, and Ixiolirion tataricum. Artemisia

baldshuanica is codominant in Amygdalus bucharica,

Pistacia vera, Otostegia bucharica, and Juniperus seravschanica communities on stony slopes (Mailun 1976).

Artemisia tenuisecta is an endemic shrub to Middle Asia

(West Tian-Shan and Pamir-Alai), about 35 to 75 cm tall,

with woody and rather thick stems, and very tomentose in

the beginning of the vegetation period (Vvedenskii 1962).

This species needs highly humid and warm weather. There

are 16 associations with this species in Uzbekistan. Their

floristic composition comprises about 136 species (Mailun

1976). Artemisia tenuisecta is codominant with Elytrigia

trichophora, Amygdalus spinosissima, Atrophaxis pyrifolia,

Rosa maracandica, Caragana alaica, Spiraea hypricifolia,

Hammada leptoclada, Prangos pabularia, Inula grandis,

Poa bulbosa, and Carex pachystylis on typical sierozems of

foothills and lower mountains (600 to 1,500 m above sea
USDA Forest Service Proceedings RMRS-P-21. 2001 111

Artemisia Communities in Arid Zones of Uzbekistan (Central Asia) Kapustina, Torrell, and Vallès

level), and with Juniperus seravschanica and J. semiglobosa

on typical brown soils. Artemisia tenuisecta communities

with Agropyron trichophorum, A. intermedium, A. setuliferum, Festuca valesiaca, Althaea nudiflora, Elytrigia

trichophora, Prangos pabularia, Inula grandis, and Amygdalus spinosissima occupy areas of mountain steppes at

heights up to 2,000 to 2,600 m above sea level. Dark sierozems are the main soils, although pale-gray and brown

mountain-steppe soils occur in under parts. Average annual

temperature is 11 to 14 °C.

Artemisia lehmanniana, A. dracunculus, and A. persica

form shrublands on the slopes and tops of the mountains

higher than 2,000 m (Akjigitova and Mailun 1984). Artemisia lehmanniana is an endemic shrub to Middle Asia, about

15 to 45 cm tall, with short, perennial, woody,very ramified

stems. Artemisia dracunculus has erect herbaceous stems

about 40 to 80 cm tall and very characteristic—very rare in

the genus—entire leaves. It occurs in Middle Asia, Siberia,

the southern part of the former Soviet Union, Minor Asia,

Afghanistan, North America, and Mongolia. Artemisia persica

is a gray-green shrub with stout woody stems. Its distribution area comprises Middle Asia, Iran, Afghanistan, and

Tibet. Those three species are codominant in Juniperus

seravschanica and J. semiglobosa communities, accompanied by Lonicera altmannii, Rosa hissarica, R. maracandica,

Malus sieversii, Acer semenovii, Adonis turkestanica, Arenaria griffithii, Phlomis olgae, and Acantholimon erythraeum.

Artemisia lehmanniana andA. persica predominate in higher

steppe mountain zones, and subalpine and alpine meadows

located between 2,800 and 3,700 m and characterized by a

significant rate of humidity (precipitation rate up to 800

mm) and a temperately cold climate with average annual

temperature of 8 °C. Soils belong to the mountain-meadowsteppe fulvous type and, less often, to the chernozem-like

subalpine type. Associations of A. lehmanniana and A.

persica with Festuca valesiaca, Cerasus verrucosa, Dactylis

glomerata, Poa nemoralis, Cousinia verticillaris, Koeleria

gracilis, Bromus inermis, and Arenaria griffithii are typical

in the steppe zone, and those with Prangos pabularia,

Ligularia thomsonii, Polygonum coriarium, Ferula tenuisecta, Cicer maracanthum, andPhlomis severtzovii are found

in subalpine and alpine meadows.

Karyology and Distribution _______

Sixteen Artemisia species form shrubland communities in

the desert and mountain zones of Uzbekistan. Most widespread communities are dominated by species belonging to

the subgenus Seriphidium: A. diffusa in the desert zone;

A. sogdiana on premountain plains and the low mountain

zone; A. tenuisecta and A. baldshuanica from foothills up to

the middle part of the mountains; and A. lehmanniana in the

higher mountain zone. These species are endemic to Middle

Asia. From a karyological viewpoint, it is worth noting that

widespread species in the desert and semidesert zones (A.

diffusa, A. sogdiana) are polyploid (2n = 36), whereas more

chorologically restricted species—adapted to xerophilous

conditions in the desert (A. turanica, A. santolina, A. leucodes)

or to more humid conditions in the mountains (A. tenuisecta,

A. juncea, A. serotina, A. porrecta)—are diploid (2n = 18).

This fact, noted by Vallès and others (2001), agrees with the

rather general assumption that polyploids usually cover

larger territories than related diploids (Ehrendorfer 1980),

even though many exceptions to this rule can be found

(Bretagnolle and others 1998).

Acknowledgments ______________

This work has been subsidized by project DGICYT (Spanish Government) PB-97-1134.

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In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Blair L. Waldron is a Research Geneticist at the Forage and Range

Research Laboratory, USDA-ARS, Logan, UT 84322-6300. R. Deane

Harrison is an NRCS Range Scientist (emeritus) at the Utah State Agricultural Expt. Station, Forage and Range Research Laboratory, USDA-ARS,

Logan, UT 84322-6300. Nicolai I. Dzyubenko is the Vice Director of Science

and Head of Forage Crops at the N.I. Vavilov Institute of Plant Industry, 42

Bolshaya Morskaya Street, 190000, St. Petersburg, Russia. Auskhan

Khusainov is the Director of the Aral Sea Experiment Station for Plant

Genetic Resources, 27 Biyekenov St., Aktyubinsk Region, Chelkar Town,

Republic of Kazakhstan, 464760. Sergey Shuvalov and Sergey Alexanian are

the Assistant Director and Director, respectively, of the Foreign Relations

Department at the N.I. Vavilov Institute of Plant Industry, 42 Bolshaya

Morskaya Street, 190000, St. Petersburg, Russia.

Kochia prostrata Germplasm Collection

Expedition to Kazakhstan

Blair L. Waldron

R. Deane Harrison

Nicolai I. Dzyubenko

Auskhan Khusainov

Sergey Shuvalov

Sergey Alexanian

Abstract—The low stature of ‘Immigrant’ forage kochia (Kochia

prostrata) limits its use as winter forage and habitat for livestock

and wildlife. In October 1999, a germplasm collection trip was

undertaken to obtain forage kochia ecotypes that have potential to

improve fall and winter forage. The collection area was north of the

Aral Sea in the Clay and Sand Desert Steppes of Kazakhstan. Seed

samples brought back to the U.S. included 192 forage kochia

ecotypes. The desert shrub ecosystems had major components of

chenopods. In general, the area was classified as Brown Desert

Steppe, Light Chestnut Steppe, Solonetz, or Degraded Solonetz.

Most soils in the Clay Desert Steppes had a clay to clay loam subsoil

and were generally saline and alkaline. Elevation ranged from 250

to 1,000 feet above sea level. Average annual precipitation was 6 to

9 inches. Average annual air and soil surface temperatures were 41

and 44 degrees Fahrenheit, respectively. On average, forage kochia

made up 6 percent of the plant composition on sites in the native

steppe where it was present, ranging from 1 to 20 percent. Forage

kochia was more prevalent when present on disturbed areas such as

abandon fields, homesteads, and roadways, where it comprised 15

to 60 percent of the plant composition. Flow cytometry analysis

revealed that 2x, 4x, and 6x ploidy levels of forage kochia were

collected.

Introduction ____________________

Forage kochia (Kochia prostrata) is a valuable semi-shrub

for rangeland rehabilitation. Some of its uses include soil

stabilization in saline/alkaline semi-arid sites, green stripping to help control wildfires, wildlife and livestock forage

and cover, and to suppress invasion of annual weeds such as

cheatgrass (Bromus tectorum) and halogeton (Hologeton

glomeratus) (Harrison and others 2000). A 3-year study

investigating the adaptability and potential for ‘weedy’

invasiveness of forage kochia was conducted by the United

States Department of Agriculture, Agriculture Research

Service (USDA-ARS), Forage and Range Research Laboratory (FRRL) in Logan, UT. Harrison and others (2000)

reported that forage kochia was widely adapted to the semiarid and arid ecosystems of the Great Basin Intermountain

Region, but was not an aggressive or weedy invader of

perennial or closed plant communities.

A forage kochia breeding and genetics program was initiated in 1998 at the USDA-ARS-FRRL in response to increasing interest in forage kochia for fall/winter livestock grazing

on privately owned land. With only one cultivar (Immigrant)

in the U.S.A. there was a lack of available germplasm to start

a breeding program. Part of the interest in new cultivars

included development of taller statured plants for improved

winter grazing and better game bird and small mammal

habitat. Because little variation had been observed in Immigrant for stature and height, scientists at the USDA-ARSFRRL attempted to obtain seed of Kazakhstan germplasm

from the N.I. Vavilov of Plant Industry. As part of a cooperative program between the U.S.A. and Russia, the USDAARS International Programs helped fund a forage kochia

collection trip to Russia and Kazakhstan.

Collection Expedition Team and

Itinerary _______________________

The collection team consisted of the six authors of this

paper and represented the USDA-ARS, N.I. Vavilov Research Institute of Plant Industry (VIR) (in Russia), and the

National Academic Center for Agricultural Research of the

Ministry of Science and Higher Education of the Republic of

Kazakhstan.

Leg 1 of the expedition consisted of a collection trip to the

South of Chelkar, Kazakhstan and East of the Aral Sea prior

to the arrival of the U.S. participants. The collection route

for leg 2, which included the U.S. participants, was to the

Kazakhstan steppe north of Chelkar, Kazakhstan. Leg 3 of

the expedition occurred after the departure of the U.S.

participants and went southwest of Chelkar (northwest of

the Aral Sea). With the exception of a listing of the species

collected and sent to the U.S. from leg 1 and 3, all other
114 USDA Forest Service Proceedings RMRS-P-21. 2001

Waldron, Harrison, Dzyubenko, Khusainov, Shuvalov, and Alexanian Kochia prostrata Germplasm Collection Expedition to Kazakhstan

details in this paper pertain to leg 2 in which the U.S.

participants were present.

The purpose of the collection trip was clearly defined in the

beginning as:

1. To expand the U.S. germplasm base of forage kochia.

2. To make a collection of forage kochia ecotypes which

would have the potential to be used in the development of a

valuable summer, fall and winter forage.

3. To continue to develop contacts and to expand upon

interactions for germplasm exchange and related agricultural research with scientists and administrators associated

with the N.I. Vavilov Institute of Plant Industry at St.

Petersburg, Russia and the Aral Sea Experiment Station for

Plant Genetic Resources at Chelkar, Kazakhstan.

While forage kochia was the primary species of interest,

additional species were collected that might fit into the same

niche as forage kochia.

Itinerary for the Second Leg

of Germplasm Collection

Expedition _____________________

The collection trip occurred in the fall of 1999 with travel

dates for the U.S. participants being October 2 to October 28,

1999. Because of logistics only 11 of those days were spent

collecting plant materials. The rest of the time was spent in

travel, visiting institutions, and preparing the seed for

export to the U.S. as outlined below.

Itinerary:

Travel Logan, UT to Moscow, Russia...Oct. 2-3

Travel Moscow, Russia to Chelkar, Kazakhstan...Oct 4-6

Collection-Chelkar, Kazakhstan northward to Karabutak,

Kazakhstan; Karabutak southeast to Irghiz, Kazakhstan;

Irghiz southwest to Chelkar, Kazakhstan...Oct 7-17

Collection-Sandy desert south of Chelkar...Oct 19

Travel Chelkar, Kazakhstan to St. Petersburg, Russia...

Oct 20-23

St. Petersburg, Russia (N.I. Vavilov Research

Institute)...Oct 24-27

Travel St. Petersburg, Russia to Logan, UT...Oct 28

Institutions Visited:

Aral Sea Experiment Station for Plant Genetic Resources, 27 Biyekenov Street, Aktyubinsk Region,

Chelkar Town, Republic of Kazakhstan, 464760.

N.I. Vavilov Institute of Plant Industry, 42 Bolshaya

Morskaya Street, 190000, St. Petersburg, Russia.

Collection Trip Results and

Summary ______________________

The expedition was very successful and 246 accessions

representing 11 species were collected (table 1). The majority of the accessions, 192, were forage kochia (Kochia

prostrata). An additional, 88 forage kochia accessions were

collected during legs 1 and 3.

Those leading the expedition told us that we were the third

U.S. collection team to visit the Aral Sea Experiment Station

for Plant Genetic Resources in Chelkar, Kazakhstan. The

two previous teams were the Westover-Enlow expedition in

1934 (N.I. Vavilov personally accompanied this expedition)

and the Asay-Johnson expedition in 1992 (Asay and others

1992). According to the Kazakhstan and Russian scientists,

our expedition route did not overlap with Asay and Johnson’s,

but unfortunately it was too late in the year to make a broad

collection of the grass species in the area. We were also told

that we were the first Americans to target forage kochia for

germplasm collection.

As experienced by Asay and Johnson in 1992, the Foreign

Relations Department (Sergey Alexanian and Sergey

Shuvalov) and other staff at VIR in St. Petersburg were

extremely cooperative, and did an excellent job of facilitating

the expedition. Dr. Nicolai Dzyubenko (Vice director of

Science and Head of Forage Crops) and Sergey Shuvalov

were primarily responsible for organizing our expedition

and accompanying us throughout the trip. Dr. Dzyubenko

had been director of the Aral Sea Experiment Station for

nine years and was familiar with the collection routes and

native vegetation. Mr. Shuvalov was fluent in English and

acted as interpreter as well as biologist on the collection

expedition. Excellent support was also provided through the

Aral Sea Experiment Station of Plant Genetic Resources in

Chelkar, which provided facilities and arranged for hiring

Table 1—Species collected during leg 1 of expedition to Kazakhstan in 1999a.

Number of Number of

Species collections Species collections

Kochia prostrata 192 Leymus [Elymus] giganta 2

Krascheninnikovia 13 Elymus angustifolius 7

[Ceratoides] papposa

Atriplex cana 8 Agropyron fragile 7

Camphorosma lessingii 10 Agropyron desertorum 2

Anabasis salsa 1 Stipa sareptana 1

Medicago falcata 3

a

In additon, 88 collections of Kochia prostrata from the first and third leg of the expedition

were brought to the United States. Additional species collected on the first tnd third legs were:

Haloxylon ammondendron—98 collections, Camphorosma lessingii—49 collections, and

Salsola orientalis—92 collections.
USDA Forest Service Proceedings RMRS-P-21. 2001 115

Kochia prostrata Germplasm Collection Expedition to Kazakhstan Waldron, Harrison, Dzyubenko, Khusainov, Shuvalov, and Alexanian

vehicles and drivers for the expedition. This experiment

station was previously under the direction of VIR, but is now

administered through the National Academic Center for

Agricultural Research of the Ministry of Science and Higher

Education of the Republic of Kazakhstan (NACAR). However, close cooperation between VIR and the experiment

station is evident. Auskhan Khusainov, director of the Aral

Sea Experiment Station for Genetic Resources, provided

excellent planning and organizational assistance for the

trip. He was directly responsible for the logistics of our travel

in Kazakhstan and accompanied us in the field, providing

taxonomic expertise on the vegetation.

Asay and Johnson noted severe budget restraints at both

VIR and the Aral Sea Experiment Station during their visit

in 1992. Funding for these institutes was even less in 1999.

The staff at the Aral Sea Experiment Station had been

reduced to the Director, Mr. Khusainov, and a few maintenance employees. There were no evaluated experimental

plots still in existence. The Vavilov Institute also was operating under severe budget restraints, but fortunately appeared to have stabilized and hopefully can rebuild its staff

and research activities during the next decade. A recent

grant from USAID had allowed them to modernize their

long-term seed storage. With the current budget restraints

they were mainly focused on germplasm collection and

preservation, and had greatly reduced their germplasm

evaluation programs. We visited staff and toured projects at

the VIR headquarters in St. Petersburg, Russia. Staff visited included Prof. Victor A. Dragavtsev, Director General of

the Institute; Dr. Sergey Alexanian, Head of Foreign Relations; Dr. Alexandr Afonin, Climatology; Dr. Vadim Molodkin,

Head of Plant Genetic Resources Long-Term Storage Laboratory; Dr. Tamara Smekalova, Herbarium; Andrew

Omelchenko, Chief of Computer-Aided Information Systems; Leonid Malyshev, Senior Scientific Researcher of the

Fodder Crops Dept.; and Antone Krylov from the Foreign

Relations office.

Environmental and Collection Details

for Leg 2

Leg 2 of the collection expedition was conducted to the

north of Chelkar. The route went as far north as Karabutak,

Kazakhstan (a few miles south of the Russian border) and

east to Irghiz, Kazakhstan. To our knowledge, we (Waldron

and Harrison) were the first Americans to make plant

collections in this area. The area had experienced a drought

and many plants appeared to be stunted. Livestock numbers

were reported to be 1⁄10 those of a decade ago, nevertheless,

we found grazing everywhere we went, with concentrated

animal numbers around villages.

Forage kochia germplasm was collected at 64 sites. These

sites were in the Clay and Sand Deserts which included the

Brown Desert Steppe, Light Chestnut Steppe, Degraded

Solonetz, and Solonetz (Atlas of Agriculture of the USSR

1960). According to scientists from the N.I. Vavilov Institute

of Plant Industry these areas have the highest concentration

of forage kochia in the former Soviet Union. Plant associations included: Agropyron–Stipa– Artemisia; Artemisia terrae-albae; Artemisia terrae-albae–Krascheninnikovia

(Ceratoides); Artemisia–Salsola–Kochia; Atriplex–Anabasis–

Artemisia; Artemisia–Anabasis; and Anabasis. Soil surface

textures included sands, fine sands, sandy loam, sandy clay

loam, silt loam, clay loam, clay, and gravelly and cobbley.

Most soils in the Clay Desert had a clay loam or clay subsoil

and were saline and alkaline. The Solonetz sites had extremely high concentrations of alkali and salt. The subsoil in

the Sandy Desert was mainly sand to fine sand. Elevations

ranged from 250 feet near the city of Irghiz to 1000 feet above

sea level north of Karabutak. Annual precipitation, averaged over 14 to 43 years, listed Chelkar at 6 to 9 inches,

Irghiz at 6 to 8 inches, and Karabutak at 10 to 12 inches

(Climate of the U.S.S.R. 1968; Agricultural management in

the Aktyubinsk region 1958). Average air and soil surface

temperatures at Chelkar are 41.9 °F and 46.4 °F, respectively; at Irghiz 41.5 °F and 44.6 °F, respectively; and at

Karabutak 37.3 °F and 41.0 °F, respectively (Climate of the

U.S.S.R. 1968).

We made 246 germplasm collections of which 192 were

forage kochia. Collections are listed by species in table 1.

Species associated with forage kochia included:

Forbs—Yarrow (Achillea micrantha), annual chenopod,

annual kochia (Kochia lanifloraand Kochia scoparia), knapweed (Centaurea picrisand other spp.), knotweed (Polygonum

spp.), buckwheat (Eriogonum sp.), fisheye (Ceratocarpus

arenarius), Russian thistle (Salsola iberica), locoweed (Astragalus sp.), and yellow flower alfalfa (Medicago falcata);

Shrubs—Artemisia austriaca, Artemisia arenaria, Artemisia terrae-albae, Salsola orientalis, winterfat (Krascheninnikovia [Ceratoides] ewersmanniana and Krascheninnikovia [Ceratoides] papposa), saltbush (Atriplex cana),

camphorosma (Camphorosma lessingii), Anabasis (Anabasis salsa), Ephreda spp., and Haloxylon aphyllum;

Grasses—Siberian wheatgrass (Agropyron fragile),

crested wheatgrass (Agropyron desertorum), needlegrass

(Stipa sareptana), giant wildrye (Leymus [Elymus]giganta),

spreading wildrye (Elymus angustifolius), Bromus inermis,

Poa spp., Festuca ovina and other Festuca spp., Stipa

capillata, reedgrass (Calamagrostis sp.), redtop (Agrostis

sp.), orchardgrass (Dactylis glomerata), saltgrass (Distichlis

sp.), tall wheatgrass (Thinopyrum ponticum), Elymus spp.,

Leymus spp., quackgrass (Elytrigia repens), foxtail (Hordeum sp.), and junegrass (Koeleria sp.).

Forage kochia on average made up 6 percent, ranging from

1 to 20 percent, of the perennial plant composition on native

steppe sites where it was present. Percentage composition

depended on the site and associated species. For example

lower percentages of forage kochia were found on the Agropyron–Stipa–Artemisia, Artemisia terrae–albae, and Artemisia–Krascheninnikovia (Ceratoides) sites while higher

percentages were found in the Artemisia–Salsola–Kochia,

and Atriplex–Anabasis–Artemisia sites. Overall, Artemisia

terrae–albae was the dominant species throughout the native steppe area. When it was present, forage kochia made

up a higher percentage of the plant composition in disturbed

areas, such as along road sides, in abandoned fields, and on

farmsteads where a high percent of annuals were present.

On these sites forage kochia ranged from 15 to 60 percent,

and averaged 32 percent of the plant composition.

As indicated above forage kochia made up a small percentage of the perennial plant communities. Nowhere on the

Kazakhstan steppes did we observe forage kochia to be

dominant in communities comprised of sagebrush, winterfat,
116 USDA Forest Service Proceedings RMRS-P-21. 2001

Waldron, Harrison, Dzyubenko, Khusainov, Shuvalov, and Alexanian Kochia prostrata Germplasm Collection Expedition to Kazakhstan

saltbush, Anabasis, crested and siberian wheatgrass, and

needlegrass. Instead, forage kochia complimented the biodiversity of such communities. In addition, we did not observe

forage kochia invading from disturbed sites into the surrounding perennial plant communities.

The forage kochia germplasm collected was mainly the

glabrous and red-green stem forage kochia (Kochia prostrata

ssp. virescens), however, some of the forms were gray with

heavy pubescence on the leaves and stems and were classified as ssp. grisea. Other forms were in-between the redgreen stem and the gray stem subspecies which indicated

that the two subspecies may hybridize. This was confirmed

by Dr. Dzyubenko and Mr. Khusainov whose combined

experience with forage kochia expands over 20 years. Seed

was collected by bulking seed from plants with similar

morphological characteristics found at the same site. The

morphological characteristics included: Height—one to three

feet; Seeds—small and large, and few to numerous; Branches

or tillers—few to numerous, and basal or high on the stem;

Leaves—mostly basal or throughout the stems and branches;

stem diameters—fine (about 1⁄16 inch) or thick stems (about 1⁄4 inch); stem color—red, yellowish-green, or gray; leaves,

branches and stem—glabrous or pubescent.

Dr. Dzyubenko and Mr. Khusainov were not aware of any

current forage kochia genetics or breeding programs in

Russia or Kazakhstan. Earlier cytogenetics work in the

former U.S.S.R. had documented diploid, tetraploid, hexaploid, and octoploid forage kochia types, and naturally occurring aneuploids resulting from hybridization between ploidy

levels. In addition, these scientists suggested that the two

subspecies of virescens and grisea, which are frequently

recognized in North American literature, are not well defined and in their native habitat readily hybridize with each

other resulting in morphological types intermediate between the subspecies. The possibility of inter-ploidy and

inter-subspecies hybridization may partially explain the

large amount of variation within forage kochia populations

at many collection sites.

The use and value of forage kochia in Kazakhstan was

discussed among trip participants throughout the trip. Obviously, forage kochia is an important part of the plant

composition throughout the northern Kazakhstan steppe

and had been heavily to moderately grazed in most of the

collection sites. It was often selectively grazed indicating

high palatability and/or high nutritional content. The number of grazing animals on the steppe has dropped to 1⁄10 the

number present at the breakup of the Soviet Union. This

greatly reduced grazing pressure and allowed us to collect

seed even in grazed areas. The numbers of grazing/browsing

animals in order of frequency were cattle, sheep and goats,

horses, camels, and Saiga (antelope). We observed utilization of forage kochia by cattle, sheep and goats, and horses,

and assumed that camels and Saiga were also grazing the

forage kochia. We observed large areas of the native steppe

that had been mowed and hayed for winter feed. Forage

kochia comprised 1 to 20 percent of that feed with Artemisia

terrae-alba being the major component and Stipa sp. and

Agropyron fragilemaking up lesser components. Even though

forage kochia made up a low percentage of the overall

biomass in the hay, we assumed that its high nutritional

value made it an important component in overwintering

livestock. We did not observe solid stands of forage kochia or

areas where it had been seeded, and in fact we only saw one

attempt to improve the steppe by seeding of any improved

forage species—a planting of crested wheatgrass. However,

Dr. Dzyubenko and Mr. Khusainov told of 20,000 ha of forage

kochia that had been planted in southern Kazakhstan. That

area was used for grazing sheep in late fall and early spring

to flush the ewes and increase the number of live births.

Evaluation of Collected Material ___

Most of the collected seed cleared quarantine and arrived

at the FRRL in mid-December, 1999. Seedlings were started

in the greenhouse in cones. Over 8,000 plants, representing

most of the forage kochia collections and some of the

Ceratoides collections were transplanted in late April (2000)

at two semi-arid locations in central and northern Utah.

Seed of 58 forage kochia entries that were sent by Dr.

Dzyubenko from the 3rd leg of the collection trip arrived too

late for the 2000 season and will be started and transplanted

in 2001.

Ploidy Level of Collected Forage Kochia

Our observations and discussions in Kazakhstan concerning ploidy levels and natural subspecies hybridization

prompted us to do a rapid test of ploidy level using flow

cytometry. Leaf samples from five plants of each collection

were bulked together and analyzed using Immigrant as a

standard.

These tests confirmed that we had collected plants of three

ploidy levels: 2x, 4x, and 6x. In some instances it appeared

that seed from plants of different ploidy levels had been

mixed together (for example, we rarely collected seed from

only an individual plant). Most surprising was the number

of collections sites where two or more ploidy levels were

coexisting (table 2). Ecological genetics would suggest that

over time one ploidy level should be most fit and eventually

displace the other ploidy levels. During the successional

phase the different ploidy levels may cross with each other

Table 2—Ploidy level of forage kochia at sites

where more than one collection was

made.

Number of sites Ploidy level observed

4 2x only

7 4x only

10 6x only

2 2x and 4x

7 2x and 6x

4 4x and 6x

6 2x, 4x, and 6x
USDA Forest Service Proceedings RMRS-P-21. 2001 117

Kochia prostrata Germplasm Collection Expedition to Kazakhstan Waldron, Harrison, Dzyubenko, Khusainov, Shuvalov, and Alexanian

resulting in aneuploidy, however, we saw very little evidence

from the flow cytometry analysis to suggest the presence of

aneuploids. These results are being verified by the USDA

Forest Service Shrub Lab in Provo, UT.

Summary ______________________

In summary, 280 collections of forage kochia were made

during a collection expedition to the Kazakhstan steppe in

October 1999. These collections greatly broaden the forage

kochia germplasm available in the U.S. and include three

ploidy levels, two subspecies, and diverse morphological

types. The collections are being evaluated at the USDA-ARS

Forage and Range Research Lab, in Logan, Utah and will be

used to develop new forage kochia cultivars for use as fall/

winter forage, greenstripping, and range reclamation.

References _____________________

Agricultural management in the Aktyubinsk region. 1958.

Kazgosizdat. Alma-Ata, Kazakhstan (In Russian).

Asay, K. H.; Johnson, D. A. 1992. Plant germplasm collection report

[Online]. Available: http://www.usu.edu/%7Eforage/russia92.htm

[verified 03 Nov. 2000].

Atlas of Agriculture of the USSR. 1960. Chief management for

geodesy and cartography. Moscow, Russia (In Russian).

Climate of the U.S.S.R. 1968. No. 18. Part H. Kazakhstan SSR.

Air humidity, precipitation, snow cover. Leningrad, Russia (In

Russian).

Harrison, R. D.; Chatterton, N. J.; Waldron, B. L.; Davenport, B. W.;

Palazzo, A. J.; Horton, W. H.; Asay K. H. 2000. Forage kochia—

Its compatibility and potential aggressiveness on Intermountain

rangelands. Utah Ag. Exp. Sta. Res. Rpt. 162. Utah State Univ.,

Logan, UT 84322-4820. pp. 66. (Available on-line: http://

agx.usu.edu/agx/ResearchReports/KOCHIA/kochia.html [verified

20 Oct. 2000]).
118 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

John H. Graham is Professor of Biology, Department of Biology, Berry

College, Mount Berry, GA 30149-0446. E. Durant McArthur is Project Leader,

Rocky Mountain Research Station, Provo, UT 84606. D. Carl Freeman is

Professor of Biology, Department of Biological Sciences, Wayne State University, Detroit, MI 48202.

Narrow Hybrid Zone Between Two

Subspecies of Big Sagebrush (Artemisia

tridentata: Asteraceae): XI. Plant-Insect

Interactions in Reciprocal Transplant

Gardens

John H. Graham

E. Durant McArthur

D. Carl Freeman

Abstract—Basin big sagebrush (Artemisia tridentata ssp.

tridentata) and mountain big sagebrush (A. t. ssp. vaseyana) hybridize in a narrow zone near Salt Creek, Utah. Reciprocal transplant

experiments in this hybrid zone demonstrate that hybrids are more

fit than either parental subspecies, but only in the hybrid zone. Do

hybrids experience greater, or lesser, use by herbivorous insects,

especially in the hybrid zone? And do certain species of herbivorous

insects prefer one or the other parental subspecies of big sagebrush?

We studied plant-insect interactions in three reciprocal transplant

gardens that span the hybrid zone at Salt Creek. Gardens were in

the basin and mountain big sagebrush zones and also in the hybrid

zone. Transplanted seedlings came from two parental and three

hybrid source populations. Densities of herbivorous insects varied

among the gardens and source populations, but the interaction

between garden and source population was statistically insignificant. Most of the variation in herbivore density was among gardens,

rather than among source populations. Only grasshoppers and

lepidopteran leaf miners showed significant preferences among the

source populations; grasshoppers preferred mountain big sagebrush and leaf miners preferred near-basin hybrids. Coccids,

Clastoptera, Trirhabda, coleophorid larvae, and lepidopteran leaf

miners showed significant differences in density among the gardens. Finally, the hybrids were not a sink for herbivorous insects,

nor did they have lower herbivore loads.

Introduction ____________________

Hybrid zones involving plants are natural laboratories for

studying the mutual adaptations of herbivorous insects and

their hosts (Strauss 1994; Fritz 1999). Thomas Whitham

(1989), working on Pemiphagus aphid galls in a Populus

hybrid zone, suggested that hybrids may often support much

greater herbivore loads than parental taxa, and by attracting herbivorous insects may hinder adaptation to the parental taxa. He called this phenomenon the hybrid sink effect.

But more recent work on a variety of plant hybrid zones has

shown that the responses of insects to hybrids and parental

taxa is not so simple, nor so general. Herbivorous insects

may indeed prefer hybrids when coadaptation for suites of

defensive chemicals has been disrupted in the hybrids, or

when hybrids are stressed (Whitham 1989; Floate and

others 1993; Morrow and others 1994; Whitham and others

1994; Christensen and others 1995; Kalischuk and others

1997). But insects may often show no preferences (Hanhimäki

and others 1994; Graham and others 1995), or may prefer

one or both parental taxa (Boecklen and Spellenberg 1990).

In a single hybrid zone, Fritz and others (1994) found that

some herbivores preferred hybrids, some preferred parentals,

and some had no preferences.

To critically evaluate plant-herbivore interactions, reciprocal transplant experiments involving plant hybrid zones

are needed (Fritz 1999). Indeed, one cannot state with

certainty that a particular species of insect prefers to feed on

a particular plant genotype unless both genotype and environment are controlled in a natural setting. In this paper, we

show that insect use of big sagebrush hybrids and parental

taxa in a reciprocal transplant experiment depends upon

both genetic differences among the big sagebrush taxa and

environmental differences across the hybrid zone. The environmental effects, however, are much stronger than the

genetic effects.

Methods _______________________

Big Sagebrush Hybrid Zone

Big sagebrush (Artemisia tridentata) is the most widely

distributed shrub in North America. Its environmental

tolerance is extreme—from arid flats to subalpine meadows.

As is true of many widely distributed species, clinal and

subspecific variation is common. And different subspecies of

big sagebrush hybridize, often in extremely narrow hybrid

zones. For example, low elevational populations of basin big

sagebrush (A. tridentata ssp. tridentata) hybridize with high

elevational populations of mountain big sagebrush (A. t. ssp.

vaseyana) wherever their distributions overlap. Introgression
USDA Forest Service Proceedings RMRS-P-21. 2001 119

Narrow Hybrid Zone Between Two Subspecies of Big Sagebrush... Graham, McArthur, and Freeman

is bidirectional (McArthur and others 1988), and the hybrids

consist of advanced generations and backcrosses.

Durant McArthur began studying sagebrush hybrids almost 25 years ago (McArthur and others 1979), and we

(including Freeman’s and McArthur’s students and colleagues) have studied the hybrid zone between basin and

mountain big sagebrush at Salt Creek, Utah, since 1989

(Freeman and others 1991). The parental taxa at Salt Creek

differ in height, stem and leaf shape, and inflorescence

structure (Freeman and others 1991), terpene and coumarin

composition (Welch and McArthur 1981; McArthur and

others 1988; Freeman and others 1991; Byrd and others

1999), and DNA markers (McArthur and others 1998b). We

have also studied herbivory and reproduction (Graham and

others 1995), developmental instability (Freeman and others 1995; Tracy and others, in preparation), and soil properties (Wang 1996; Wang and others 1998). In 1993, we began

a reciprocal transplant experiment in the Salt Creek hybrid

zone. This experiment was designed to critically test the

predictions of three hybrid zone models: the dynamic equilibrium model, the mosaic hybrid zone model, and the

bounded hybrid superiority model.

The big sagebrush hybrid zone at Salt Creek is best

explained by the bounded hybrid superiority model (Wang

and others 1997). This model suggests that hybrids have the

highest reproductive fitness, but only in the hybrid zone

(Moore 1977). The competing dynamic equilibrium model

maintains that hybrid zones are stabilized by selection

against hybrids, and by gene flow across the zone (Barton

and Hewitt 1985); the hybrid zone is independent of the

environment. And the mosaic hybrid zone model maintains

that exogenous selection acts against hybrids, but that

parental taxa are adapted to different environments

(Harrison and Rand 1989; Arnold 1997).

Studies in the transplant gardens at Salt Creek have

included reproductive fitness (Wang and others 1997; Freeman and others 1999), respiration and water potential

(McArthur and others 1998a), nutrient uptake (Wang 1996;

Wang and others 1999), and growth (Freeman and others

1999). These studies are summarized in Graham and others

(1999). Current research involves taxon-specific soil mycorrhizal associations (Miglia and others, unpublished data)

and developmental stability (Graham and others, unpublished data). Graham and others (1995) studied the distribution and use of big sagebrush by gall-formers, grasshoppers,

aphids, and deer in the hybrid zone, but this research did not

involve the transplant gardens. Messina and others (1996)

looked at insects on hybrid and parental sagebrush grown in

a single common garden, but the garden was not actually in

a hybrid zone.

Study Site

The reciprocal transplant gardens span the big sagebrush

hybrid zone at Salt Creek, near Nephi, Utah (Uinta National

Forest, Juab Co., Fountain Green North Quadrangle). Basin

big sagebrush occur along Salt Creek and its tributaries, to

an elevation of about 1,790 m. Mountain big sagebrush occur

from about 1,850 m to timberline on nearby Mt. Nebo. The

hybrids occur from 1,790 to 1,830 m elevation, in a narrow

band between the basin and mountain populations (Freeman and others 1991).

We studied five stands of big sagebrush at Salt Creek: the

two parental subspecies and three classes of hybrids. We

refer to A. t. ssp. tridentata as basin, A. t. ssp. vaseyana as

mountain, the middle hybrid as hybrid, the hybrid between

basin and middle hybrid as near basin, and the hybrid

between mountain and middle hybrid as near mountain.

Reciprocal Transplant Gardens

We germinated seeds from the five source populations

(basin, near basin, hybrid, near mountain, and mountain),

grew the seedlings for one year in a greenhouse, and planted

twelve seedlings from each source in each of three gardens

(basin, hybrid, mountain) during May 1993. The gardens

were enclosed with 2.5 m high fences, for protection from elk,

deer, and cattle.

The basin garden is on a bench just above the flood plain

of Salt Creek, at an elevation of 1776 m. The mountain

garden is on the lower slope of Mt. Nebo, at an elevation of

1870 m. The hybrid garden is in a relatively flat meadow, at

an elevation of 1800 m, and midway between the basin and

mountain gardens. (See Wang and others [1997] for additional details.)

Census of Insects

We counted insects on big sagebrush in our three gardens

during the week of June 21-27, 1997. Although this is a

relatively brief sampling period, it occurs at a time of year

when insect activity on sagebrush is at a peak. Respiration

rates and water potential reach their seasonal peaks in early

summer (McArthur and others 1998a), and temperatures

are not yet warm enough to restrict insect activity. For

grasshoppers, we counted both the insects and the physical

evidence of their browsing. And because the ant Formica

dakotensis montigena makes its nest below ground, at the

base of sagebrush, we only recorded its presence or absence

on a plant. Samples of all insects were preserved in 70

percent ethanol for later identification.

Plant size may influence numbers and diversity of insects.

To estimate density of herbivores, we needed an estimate of

relative plant volume. A measure of volume is v = hc2 , where

h is height and c is crown diameter. This is a measure of the

volume of the smallest square-ended box enclosing a plant.

Statistical Analysis

Plant size varied among gardens and taxa, so we expressed all counts as densities (i.e. number divided by v). We

used MANOVA to compare insect densities of the most

common insect species among gardens and source populations. We used a crossed design, with replication. Individual

plants (the replicates) were nested within the garden by

source population. Both garden and source were fixed variables in the MANOVA. A separate MANOVA was done for

the three main guilds of insects: chewers, suckers, and gallformers. (Data on the gall-formers is from Graham and

others 2001). As an adjunct to the MANOVAs, we also

performed univariate two-way ANOVAs for each variable.

We used analysis of covariance (ANCOVA) to compare insect

diversities among gardens and source populations.
120 USDA Forest Service Proceedings RMRS-P-21. 2001

Graham, McArthur, and Freeman Narrow Hybrid Zone Between Two Subspecies of Big Sagebrush...

Most of the insects on sagebrush had contagious (clumped)

distributions. Southwood (1978) recommends a logarithmic

transformation for highly contagious distributions. We found

that a logarithmic transformation of the densities (log10 [x + 1])

gave the best approximation to a normal distribution, and

stabilized the variance.

Results ________________________

Herbivore Density and Distribution

Herbivorous insects on big sagebrush included several

orthopterans, homopterans, lepidopterans, and coleopterans (table 1). Dipteran gall-formers, which were also present,

are treated in a separate paper (Graham and others 2001).

There were significant differences in densities of herbivores among the three gardens and five source populations

(table 2). The effect of garden, however, was more highly

significant than that of source population. Five herbivores

(coccids, spittlebug larvae, Trirhabda pilosa, coleophorid

larvae, and leaf miners) differed significantly among gardens, while only two species (grasshoppers and leafminers)

differed significantly among source populations. Gardens by

source population interactions were insignificant.

Herbivorous insects fall into three feeding guilds: leaf

chewers and miners, phloem and xylem suckers, and gallformers. Leaf chewers include the grasshoppers, chrysomelid

beetles, and lepidopteran larvae. Grasshoppers (Melanoplus

sp. and other species) were in low densities in all three

gardens, but preferred mountain big sagebrush (fig. 1).

Both larval and adult chrysomelids fed on big sagebrush.

Trirhabda pilosa has a metallic-green larva that can inflict

significant damage on sagebrush. The larvae were only on a

few plants in the hybrid garden. In contrast, the adults were

only in the basin garden (fig. 2). The larva and adult Exema

conspersa feed on leaves. Their densities did not vary among

gardens or source populations (table 2 and fig. 2). Other

coleoptera, such as weevils (Sternechus sp.) and scarabid

beetles, (Dichelonyx sp.) were rare.

Larval lepidoptera included a pterophorid moth, a casebearing coleophorid moth, and an unidentified leaf miner.

All three species feed on leaves. While the pterophorids were

uncommon, the more abundant coleophorids differed significantly among gardens (table 2), and were most abundant in

the basin garden (fig. 3). Leaf miner densities varied among

gardens and source populations (table 2). They were more

abundant in the mountain garden, and preferred near-basin

plants (fig. 3).

Phloem and xylem suckers include the aphids, coccids,

spittlebugs, leafhoppers, cicadas, and true bugs. Two species

of aphids were Obtusicauda coweni and O. filifoliae. Neither

showed significant differences in density among gardens or

source populations (table 2 and fig. 4). Coccids (scale insects)

showed significant differences among gardens (table 2).

They were most common in the basin garden, absent from

the mountain garden, and of intermediate abundance in the

hybrid garden (fig. 5). Spittlebugs (Clastoptera sp.) showed

significant variation among gardens (table 2). They were

also most abundant in the basin garden (fig. 5). Leafhoppers,

cicadas, and true bugs (Lygus sp.) were rare.

Table 1—Insects found on big sagebrush in the reciprocal transplant gardens.

Scientific name Family: Order Description

Herbivorous Insects

Melanoplus sp. Acrididae: Orthoptera Browsing on stem

Unknown grasshoppers Acrididae: Orthoptera Browsing on stem

Obtusicauda coweni Aphididae: Homoptera Black phloem-feeding aphid

Obtusicauda filifoliae Aphididae: Homoptera Green phloem-feeding aphid

Scale Insect Coccidae: Homoptera Phloem feeder

Clastoptera sp. Cercopidae: Homoptera Phloem-feeding nymph

Leafhopper Cicadellidae: Homoptera Phloem feeder

Cicada Cicadidae: Homoptera Phloem feeder

Lygus sp. Miridae: Hemiptera Phloem feeding larva and adult

Sternechus sp. Curculionidae: Coleoptera Leaf chewing adult

Trirhabda pilosa Chrysomelidae: Coleoptera Leaf chewing larva and adult

Exema conspersa Chrysomelidae: Coleoptera Case-bearing larva and

leaf chewing adult

Octinodes sp. Elateridae: Coleoptera Non-feeding adult

Dichelonyx sp. Scarabaeidae: Coleoptera Leaf chewer

Lyctus sp. Lyctidae: Coleptera Wood borer

Moth larva Pterophoridae: Lepidoptera Leaf chewing caterpillar

Casebearing moth Coleophoridae: Lepidoptera Leaf chewing caterpillar

Unidentified moth larva Lepidoptera Leaf miner

Non-herbivorous Insects, and other Arthropods

Hippodamia apicaulis Coccinellidae: Coleoptera Ladybird beetle

Formica dakotensis Formicidae: Hymenoptera Nest at base of plant

Monomorium minimum Formicidae: Hymenoptera Tending coccids

Wasp Hymenoptera

Spider Aranae
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Narrow Hybrid Zone Between Two Subspecies of Big Sagebrush... Graham, McArthur, and Freeman

Table 2—Multivariate and univariate ANOVAs for the effects of garden,

source, and garden by source interaction on density of

herbivorous insects.

MANOVA

Source Df Wilks’ λ F P

Garden 18, 240 0.28962 11.44244 <0.001

Source 36, 451 0.66124 1.46339 0.044

Garden x Source 72, 737 0.49543 1.25367 0.083

Univariate ANOVAs (F statistics)

 Effect (degrees of freedom in parentheses)

Garden Source Garden x Source

Insect (2, 128) (4, 128) (8, 128)

Acrididae 2.564 2.495 * 1.275

Obtusicauda coweni 0.888 2.091 1.240

Obtusicauda filifoliae 1.718 0.638 0.733

Coccidae 10.239 *** 1.283 1.627

Clastoptera sp. 7.480 ** 0.660 1.908

Exema conspersa 1.914 1.238 0.488

Trirhabda pilosa 6.266 ** 2.327 1.561

Coleophoridae, larva 4.488 * 0.276 0.873

Leaf Miners 95.587 *** 3.393 * 1.976

* P <0.05.

** P <0.01.

*** P <0.001.

Figure 1—Interaction of garden and source population on density of hoppers and hopper browse. Source

populations are B (basin), NB (near basin), H (hybrid),

NM (near mountain), and M (mountain).

Figure 2—Interaction of garden and source population

on density of coleopteran adults and larvae of Exema

conspersa and Trirhabda pilosa. Source populations

are B (basin), NB (near basin), H (hybrid), NM (near

mountain), and M (mountain).
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Graham, McArthur, and Freeman Narrow Hybrid Zone Between Two Subspecies of Big Sagebrush...

Figure 3—Interaction of garden and source

population on density of coleophorid larvae and

lepidopteran leaf miners. Source populations

are B (basin), NB (near basin), H (hybrid), NM

(near mountain), and M (mountain).

Figure 4—Interaction of garden and

source population on density of aphids

Obtusicauda coweni and O. filifoliae.

Source populations are B (basin), NB

(near basin), H (hybrid), NM (near

mountain), and M (mountain).
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Narrow Hybrid Zone Between Two Subspecies of Big Sagebrush... Graham, McArthur, and Freeman

Table 3—Multivariate and univariate ANOVAs for the effects of garden,

source, and garden by source interaction on density of three

guilds. Data on galls is from Graham and others (2001).

MANOVA

Source Df Wilks’ λ F P

Garden 6, 252 0.17658 57.95019 <0.001

Source 12, 334 0.71593 3.74334 <0.001

Garden x Source 24, 366 0.71834 1.84275 0.010

Univariate ANOVAs (F statistics)

 Effect (degrees of freedom in parentheses)

Garden Source Garden x source

Guild (2, 128) (4, 128) (8, 128)

Chewers and miners 90.257 *** 4.268 ** 2.488 *

Suckers 0.179 0.759 1.100

Gall-formers 128.935 *** 6.340 *** 2.202 *

* P <0.05.

** P <0.01.

*** P <0.001.

Figure 5—Interaction of garden and source population

on density of coccids and spittlebug (Clastoptera sp.)

larvae. Source populations are B (basin), NB (near basin),

H (hybrid), NM (near mountain), and M (mountain).

The three guilds (leaf chewers and miners, phloem and

xylem suckers, and gall-makers) showed significant differences in density among gardens and source populations

(table 3). (Data on gall-formers is from Graham and others

[2001]). There was also a significant garden by source

population interaction (fig. 6). Gall-makers were the most

abundant of the three guilds; phloem suckers were the least

abundant. Densities of galls and leaf chewers and miners

were highest in the mountain garden, but varied with source

population (fig. 6). Phloem suckers did not differ significantly among gardens or source populations (table 3).

Herbivore Diversity

Do garden and source population have an effect on species

diversity of herbivorous insects? Because the size of a plant

may also influence the species diversity of insects, we used

analysis of covariance to eliminate the effect of plant size.

The effect of plant size (log10 [v + 1]) on species diversity

(log10 [S + 1]), where S is the number of species, was both

linear and homogeneous with respect to garden, source, and

garden by source, for herbivores.

Diversity of herbivorous insects depends upon both shrub

size and garden (table 4). The number of herbivorous species

increased with increasing plant volume (b = 1.4695, t = 2.661,

P = 0.009). And the hybrid garden had fewer species of

herbivorous insects than either the basin or mountain gardens (fig. 7).

Incidental Nonherbivores

The nonherbivorous arthropods included two species of

ants (Formica dakotensis montigenaand Monomorium minimum). Formica d. montigena nested under leaf thatch below

the canopy, and around the trunk, of individual plants.

These large red and black ants vigorously defended their

nests, and plants. Formica dakotensis was more common in

the mountain garden, but showed no obvious preference for

sagebrush from any of the five source populations. Presence

of a Formica nest at the base of a plant had no effect on the

diversity of herbivores and galls (MANCOVA, F 2, 139= 0.088,

P = 0.916) or on the density of leaf chewing insects and

sucking insects (MANCOVA, F 2, 137 = 0.802, P = 0.451). The

smaller black ant (Monomorium minimum), restricted to

the basin garden, was usually associated with, and tending,

coccids. Its density was correlated with coccid density

(r = 0.5339, df = 142, P <0.001), but not with aphid density

(r = 0.0338, df = 142, P >0.50).

Several predatory arthropods were present on the sagebrush. The ladybird beetle Hippodamia apicaulis was fairly

common, as were several species of unidentified spiders. The

click beetle (Octinodes sp.) and lyctid wood borer (Lyctus sp.)

were rare. Occasional wasps were seen, but not collected.
124 USDA Forest Service Proceedings RMRS-P-21. 2001

Graham, McArthur, and Freeman Narrow Hybrid Zone Between Two Subspecies of Big Sagebrush...

Table 4—Analysis of covariance for the effects of garden and source

population on diversity of herbivorous insects (log10 [S + 1]).

Plant volume (log10 [v + 1]) is the covariate.

Source Df MS F P

Garden 2 0.23 8.09 <0.001

Source 4 0.01 0.49 0.743

Garden x Source 8 0.02 0.87 0.545

Size 1 0.20 7.08 0.009

Discussion _____________________

Densities of herbivorous insects on hybrid and parental

big sagebrush vary with both genotype and environment.

Messina and others (1996) found that herbivore use of

hybrid and parental big sagebrush in a common garden in

northern Utah depended upon plant genotype. Our experiment extends their results by examining hybrids and

parentals in reciprocal transplant gardens that span an

actual hybrid zone. Of the two main effects, environment

(garden) had a greater effect on herbivore density than did

genotype (source population). We found the same pattern for

gall-formers (Graham and others 2001). Nevertheless, gallformers showed significant genotype-environment interactions, while none of the individual species of chewers and

suckers did.

Figure 6—Summary of interactions of garden and source population on densities of leaf chewers and miners, and

phloem suckers. Source populations are B (basin), NB (near basin), H (hybrid), NM (near mountain), and M (mountain).

Figure 7—Interaction of garden and source population on diversity of herbivorous insects, after removing

the effect of plant volume on diversity. Source populations are B (basin), NB (near basin), H (hybrid), NM

(near mountain), and M (mountain).
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Narrow Hybrid Zone Between Two Subspecies of Big Sagebrush... Graham, McArthur, and Freeman

Among the herbivorous insects, only the grasshoppers

and leaf miners showed any evidence of host specificity.

Grasshoppers were absent from near-mountain plants, but

this may result from sampling bias, since their densities

were low. Leaf miners clearly preferred near-basin plants,

but they were present on all five populations.

Aphids of the genusObtusicauda are Artemisia specialists

(Robinson and Halbert 1989). Graham and others (1995)

found more aphids on middle and near-mountain hybrids in

1989. Nevertheless, in 1997 we found no evidence of specialization on hybrids or parental subspeciesbyeither O. filifoliae

or O. coweni. Obtusicauda coweni and O. filifoliae were

equally common in all three gardens, and showed no preferences among the five source populations. Greater densities

of aphids on hybrids in 1989 may have been related to

rainfall patterns in that year, and also to the time of year the

aphids were censused (August). In July, water potential of

sagebrush is still high in all three gardens, but by September, plants in the mountain garden are experiencing greater

water stress than those in either the hybrid or basin gardens

(McArthur and others 1998a). Low water potential can

reduce sap intake by aphids, resulting in lower reproductive

potential or movement to new plants (Kennedy and Stroyan

1959). Thus, in some years spatial and temporal variation in

aphid density and distribution may result from environmental and temporal variation in water availability (Moran and

Whitham 1988).

Herbivorous insects may severely affect the fitness of

individual plants. The chrysomelid beetle Trirhabda pilosa

can defoliate and kill entire populations of big sagebrush,

especially at higher elevations (Pringle 1960). Both larvae

and adults are leaf chewers. We found no evidence of such

high population densities in our gardens. In the 10 years we

have studied the hybrid zone at Salt Creek, we have not seen

defoliation by Trirhabda. Only a small number of plants

were infested with either larvae (in the hybrid garden) or

adults (in the basin garden). The distribution of larvae and

adults in the hybrid and basin gardens is probably related to

timing of emergence. After reaching a length of about 10

mm, larvae drop off the host plant, pupate in the soil, and

emerge as adults 1 to 2 weeks later (Pringle 1960). In August

1998, we observed many adults in the mountain garden, so

we were probably sampling too early in 1997 to find larvae

or adults in the mountain garden.

Incidental arthropods may have a significant influence on

plant-herbivore interactions. Ants often interact with aphids,

and in the process reduce herbivory by leaf-chewing insects

(Pringle 1960; Floate and Whitham 1994). They also prey on

ovipositing Rhopalomyia (Jones and others 1983). We did

not, however, find a significant association of Formica

dakotensis or Monomorium minimum with aphids, nor a

negative association with either galls or leaf chewing insects. This is true despite the fact that Formica vigorously

defended individual plants. Formica dakotensis is a temporary social parasite on the F. fuscus group (Wheeler and

others 1994). Formica obscuripes, another member of the

rufa group, also nests under sagebrush, and is known to kill

and remove the plant from its nest (Cole 1932, as cited by

Creighton 1950). According to Robinson and Halbert (1989),

Obtusicauda aphids are not tended by ants. Monomorium

minimum was found tending scales, rather than aphids.

Conclusion_____________________

Only grasshoppers and leafminers appear to distinguish

among hybrid and parental genotypes. Coccids, Clastoptera,

Trirhabda pilosa, coleophorid larvae, and lepidopteran leaf

miners, on the other hand, all show more significant variation among environments. Most importantly, hybrids in the

big sagebrush hybrid zone are not more heavily grazed than

the parental taxa; the hybrid zone is not a sink for herbivores. Nor do they experience less grazing than the parental

taxa in the hybrid zone. Insects vary along the elevational

gradient, and a few also seem to target particular taxa.

Acknowledgments ______________

Catherine Chamberlin-Graham helped with the insect

census and did the literature search; she also proofread the

final draft of the manuscript. Susan Halbert identified the

aphids. Gary Jorgensen assisted in the maintenance of the

experimental gardens. This research was partially funded

by a faculty development grant from Berry College.

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D. Carl Freeman is a Professor of Biological Sciences at Wayne State

University in Detroit, MI. John H. Graham is an Associate Professor at Berry

College in Rome, GA. Terra Jones is an Undergraduate Student at Wayne

State University. Han Wang is a Post Doctoral Fellow at the University of

Oregon. Kathleen J. Miglia is a Graduate Student at Wayne State University

and E. Durant McArthur is the Project Leader at the U.S. Forest Service

Shrub Sciences Laboratory in Provo, UT.

Abstract—Reciprocal transplant studies in the big sagebrush

hybrid zone at Salt Creek Canyon, Utah, showed that hybrids

between basin (Artemisia tridentata ssp. tridentata) and mountain

big sagebrush (A. t. ssp. vaseyana) are more fit than either parental

taxon, but only when raised in the hybrid zone. Hybrids are less fit

than the native parent when raised in the parental environments.

Why this is the case remains an open question. Our earlier work has

shown that the hybrid zone occurs in an ecotone where the soil,

vegetation, and herbivorous insect community all differ markedly

from that found in the parental habitats. Moreover, the spatial

variation in soil chemistry was greater in the hybrid zone than in

either parental habitat. Does the enhanced genetic variation that

results from hybridization allow hybrids to adapt to hyperspatial

variability within the hybrid zone? Here we used Euclidean distance measures to examine this question for sagebrush hybrid zones

found at Salt Creek and Clear Creek Canyons in Utah. Specifically,

we examine the spatial variation in soil chemistry, vegetation, and

insect communities. We also explore the interplant variability in the

production of terpenes, ten elemental leaf concentrations, and the

plants’ biological absorption coefficients. While the hybrid zone is

spatially more variable for soil chemistry, it is not more variable in

terms of the vegetation nor herbivorous insects. Spatial variation

for these features of the environment was greatest in the mountain

zone, least in the basin zone and intermediate in the hybrid zone. In

all three gardens overall, hybrid plants displayed greater variation

than either parental taxon, in terms of their leaf elemental chemistry and biological absorption coefficients. However, the variability

for all parental and hybrid plants increased when raised in alien

gardens.

Use of Distance Measures to Assess

Environmental and Genetic Variability

Across Sagebrush Hybrid Zones

D. Carl Freeman

John H. Graham

Terra Jones

Han Wang

Kathleen J. Miglia

E. Durant McArthur

Introduction ____________________

The bounded hybrid superiority model postulates that

the maintenance of stable hybrid zones is due to genotypeby-environment interactions. Accordingly, the parental taxa

and hybrids each have superior fitness in their native

habitats. Hybrids are presumed to be more fit within the

hybrid zone, but less fit outside it, compared to either

parental taxon. Reciprocal transplant experiments are required to test this model, as descriptive studies or single

common-garden experiments confound genetic and environmental effects, thereby preventing assessment of genotypeby-environment interactions. Recently, a number of reciprocal transplant experiments have been conducted with plants

(Young 1996; Wang and others 1997; Emms and Arnold

1997). These studies found that the fitness of hybrids was

generally equal or superior to that of the parental taxa

within the hybrid zone, but less fit than either parental type

outside the hybrid zone. This was most evident when estimates were made using composite fitness parameters (Wang

and others 1997).

Why should superiority of hybrid fitness be confined to

within the margins of the hybrid zone? As Kettlewell (1956)

demonstrated, fitness can be a function of both genotype

and the environment, so the above question actually comprises three different questions: (1) what is special about the

environment of the hybrid zone? (2) why should hybrids

exhibit superior fitness in this unique environment compared to the parental taxa? and (3) why can’t hybrids expand

their range and thereby displace the parental taxa?

While considerable attention has been given to the genetic

analysis of hybrid zones (see Arnold 1997 for an excellent

review), ecological analyses have received much less attention. Most ecological work has focused on the influence of

plant hybrid zones on herbivore distribution and abundance

(Whitham and others 1999; Pilson 1999; Moula 1999; Fritz

1999, and references therein). These studies are fascinating,

but they do not address the issues raised here because the

environment is not examined from a plant’s perspective.

We have adopted an ecological approach to our study of the

big sagebrush hybrid zone. A number of features relevant to

the performance of plants (in other words, soil mineral

composition and the distribution and abundance of other
128 USDA Forest Service Proceedings RMRS-P-21. 2001

Freeman, Graham, Jones, Wang, Miglia, and McArthur Use of Distance Measures to Assess Environmental and Genetic Variability...

plant species and herbivorous insects) have been investigated (table 1). Profiles of defensive chemicals produced by

the plants have also been examined. Thus far, these

studies have supplied partial answers to the above three

questions.

We have shown that the hybrid zone occurs in an

ecotone. Specifically: (1) soil chemistry differs radically

between the parental sites and parental habitat soils differ

markedly from that of the hybrid zone; (2) soils from the

hybrid zone are not just intermediate blends of the parental habitat soils, but have their own unique properties;

(3) plant species composition and vegetation (estimated as

percent of ground cover) differ significantly between the

parental sites and these sites also differ from the hybrid

zone; and (4) vegetation in the hybrid zone community is not

a simple blend of that in the parental communities, but

rather includes some unique species. In short, both soil

chemistry and vegetation have unique features in the

hybrid zone, to which the hybrids have adapted. However,

hybrids are maladapted to the environmental conditions

existing in either parental zone (Wang and others 1997).

Why hybrids, and not the parental taxa, are adapted to the

unique features of the hybrid zone (question 2) remains

open.

In an earlier paper (Wang and others 1998), Euclidean

distance measures showed that the big sagebrush hybrid

zone is spatially more variable in soil elemental composition

than either parental site (fig. 1). This suggests that the

enhanced genetic variation resulting from hybridization

may be necessary to cope with the increased spatial variation of soil chemistry within the hybrid zone. The present

study extends that analysis to examine the variability in

vegetation, insect herbivore loads, and terpene profiles of

leaves. Interplant variability is also examined for plants

raised in common gardens, using elemental leaf concentrations and the ratio of elemental leaf to soil concentrations (in

other words, the biological absorption coefficients, BACs).

This latter analysis examines how the variability among

plants changes when the plant is raised in a nonnative

environment.

Table 1—Sources of data used in this paper.

Insect Community Composition Graham and others, 2001; Graham and others, this proceedings

Plant Chemistry Wang and others 1999

Plant Community Composition Freeman and others 1999

Plant Developmental Instability Freeman and others 1995

Plant Terpenes Byrd and others 1999

Soil Chemistry Wang and others 1998

Figure 1—MAD and CRD distances based upon soil chemistry for both the Salt Creek and Clear Creek hybrid zones.

Basin Near

Basin

Middle

Hybrid

Near

Mountain

Mountain

MAD Salt Creek

200

180

160

140

120

100

80

60

40

20

0

Soil MAD

Basin Near 

Basin

Near 

Mountain

Mountain

MAD Soil Clear Creek

165

160

155

150

145

140

135

130

125

120

Soil MAD

Basin Near

Basin

Middle

Hybrid

Near

Mountain

Mountain

CRD Salt Creek

0.2

0.15

0.1

0.05

0

Soil CRD

Basin Near 

Basin

Near 

Mountain

Mountain

CRD Clear Creek

0.14

0.12

0.1

0.08

0.06

0.04

0.02

0

Soil CRD





    











 








USDA Forest Service Proceedings RMRS-P-21. 2001 129

Use of Distance Measures to Assess Environmental and Genetic Variability... Freeman, Graham, Jones, Wang, Miglia, and McArthur

Methods _______________________

Methods for a specific data collection are given in the

primary article dealing with that subject (table 1). We have

primarily conducted our studies in Utah at both Salt Creek

and Clear Creek Canyons. Salt Creek Canyon is located at

the south end of the Wasatch Mountains near Nephi, whereas

Clear Creek Canyon is located near Richfield and drains the

east slope of the Pavant and Tushar Mountains. Sampling in

both study areas occurred across the hybrid zone in native

vegetation; however, data was also collected from three

experimental gardens established in Salt Creek Canyon

(one in each parental population and one in the middle of the

hybrid zone—see Wang 1996). In the native vegetation at

Salt Creek Canyon, five sampling sites were established

(one in each parental population and three within the hybrid

zone), while four were established at Clear Creek Canyon

(one in each parental population and two within the hybrid

zone). Soil chemistry was assessed at both sites, whereas

vegetation was only assessed at Clear Creek Canyon because

portions of Salt Creek Canyon have been seeded with alien

grasses. Cattle grazing occurs at both locations. Terpene

profiles and insect abundance were analyzed for transplantgarden plants at Salt Creek Canyon. Leaf chemistry was

also addressed using plants indigenous to a site.

Euclidean distance was used to measure spatial environmental heterogeneity. Specifically, to examine differences

due to magnitudes, the mean absolute Euclidean distance

(MAD) was determined by applying the following equation

(Freeman and others 1995):

MAD = S Xij-Xik S

Using soil chemistry as an example, Xij is the measure of

the magnitude of the ith element in sample j, Xik represents

the concentration of the same element in sample k, and S

represents the number of elements included in the distance estimate. We measured the concentrations of 10

elements in the soil, so, in this case, S = 10. The concentration of each element forms an axis in the analysis, and the

distance between the samples is a measure of their dissimilarity. This distance is summed for each axis and then

divided by the number of elements to yield the MAD estimate. Chord distance (CRD) is similar, but examines proportions rather than absolute amounts:

CRD = s 2(1-ccosjk)

where ccosjk = S (Xij Xik)

sS X2

ijSX2ik

In brief, the distance between samples is projected onto a

unit circle and the chord that separates the two samples is

a measure of the dissimilarity in the proportion of elements

measured in the soils. Vegetation, terpenes and leaf chemistry were treated in a similar manner.

Data Analysis

When analyzing the distances for vegetation, terpenes, and

herbivore loads, a Kruskal-Wallis test was used because the

data did not conform to the assumptions of an ANOVA (Zar

1984). However, ANOVAs were used to analyze elemental leaf

concentrations and their biological absorption coefficients.

Results ________________________

Soil Chemistry

Soil chemistry plays such an important role in the

present study that we will summarize the results of

Wang and others (1998). Both MAD and CRD distances

differed significantly among the sites at Salt Creek Canyon

(χ2 > 40.0 P < 0.00001 in both cases) (fig. 1). MAD distances

at the basin site were significantly less than at the middlehybrid site, but not at the near-basin or mountain sites. The

near-basin and mountain sites did not differ significantly

from the middle hybrid or near-mountain sites. CRD distances differed significantly between the basin and four

other sites at Salt Creek Canyon. At Clear Creek Canyon,

MADs did not differ among the sites, but CRDs did (χ2

 >

40.0). The mean CRD at the mountain site was significantly

less than at the other three sites, while the mean CRD at the

near-mountain site was significantly greater than the means

at either the basin or near-basin site. This indicates that at

Salt Creek Canyon, both the concentrations and proportions

of elements in the soils were spatially more variable in the

hybrid zone than at the basin site. While the spatial variability was greater in the hybrid zone than at the mountain site,

the difference was not significant. At Clear Creek Canyon,

the spatial variation in the proportion of elements was

greater in the hybrid zone than at the mountain site.

Vegetation

MADs differed significantly among the sites (χ2 = 23.4, P

< 0.000034, table 2). Mean MAD at the basin site was

significantly greater than at the other three sites, while

these sites did not differ from one another. This indicates

that quadrats in the basin site had greater disparity in the

amount of vegetation than that occurring at the other sites.

CRD distance also differed significantly among the sites

(χ2 = 135.0, P < 0.000001). The mean CRD at the basin site

was significantly less than that at the near-basin and mountain sites, but did not differ from that at the near-mountain

Table 2—Analysis of spatial heterogeneity of the vegetation using Euclidean distance measures at the Clear

Creek Site. The MAD examines differences among quadrats in the amount of vegetation while the

CRD examines differences in the proportion of vegetation contributed by each species. Means

subscripted by the same letter do not differ significantly from one another at the 0.05 level.

Basin Near basin Near mountain Mountain χ2 P

MAD 2.21a 1.75b 1.88b 1.85b 23.37 0.000034

CRD 0.96a 1.05b 0.94a 1.25c 134.99 0.000001
130 USDA Forest Service Proceedings RMRS-P-21. 2001

Freeman, Graham, Jones, Wang, Miglia, and McArthur Use of Distance Measures to Assess Environmental and Genetic Variability...

site. Mean CRD at the near-basin site was significantly

greater than that at the near-mountain site, but significantly less than that at the mountain site. Mean CRD at the

mountain site was significantly greater than that at the

other three sites. Collectively, these results indicate that the

proportion of vegetation contributed by a species was remarkably uniform at the basin site, but that the density of

vegetation there varied greatly among the quadrats. While

at the mountain site, the amount of vegetation was quite

constant but the composition of the vegetation varied greatly

among the quadrats. Thus, by either measure, the parental

sites are more variable than either hybrid site.

Insects

MADs were examined for plants in the common gardens.

The data were not normally distributed, so a Kruskal-Wallis

test was used for this analysis. A single coding variable was

also used to indicate both garden and source populations

(table 3). As there are three gardens and five source populations, this coding variable had 15 states. MADs differed

significantly among these 15 states (χ2= 571.9, P < 0.000001).

In general, two major trends are evident: (1) the siteindigenous population always had the smallest MAD and

(2) hybrids had greater MADs than the parental taxa (this

trend is more evident in the parental gardens, though the

nonindigenous hybrids had higher MADs even in the hybrid

garden). The mean CRDs also varied significantly among

the 15 states of the coding variable (χ2= 214.4, P < 0.000001).

In general, the mean CRD was lowest in the basin garden

and highest in the mountain garden, with basin plants

having lower CRDs than mountain plants. One form of

hybrid had the highest CRDs in the basin and hybrid

gardens, but not in the mountain garden where mountain

plants had the highest CRD. Thus, the total density of

insects appears to be most variable on the nonsite indigenous and hybrid plants. Like the vegetation, the proportional contribution of an insect species to the total herbivore

load was more uniform in the basin than mountain garden. In the basin and middle-hybrid gardens the proportions of insect species varied most among the hybrids, but

in the mountain garden, native parental plants had greater

variability.

Terpenes

MADs differed significantly among the five sampling

locations at Salt Creek Canyon (χ2 = 42.8, P < 0.000001)

(table 4). Mean MAD at the basin site was significantly less

than that at the near-mountain and mountain sites. No

other differences were significant. CRDs did not differ among

the sites (χ2

 = 0.4, P = n.s.).

Leaf Chemistry

Site Indigenous Plants—Leaf chemistry was examined

for both site-indigenous and transplant-garden plants. For

site-indigenous plants, MADs were significantly greater for

the basin and middle-hybrid plants than for the mountain

and near-basin plants. Near-mountain plants were intermediate (table 5). CRDs also differed significantly among the

sites (F 4,135 = 4.19 P, < 0.003, table 5 and fig. 2). CRDs were

greatest for the middle-hybrid and basin plants and lowest

for near-basin and mountain plants. MADs based on the

biological absorption coefficient also differed significantly

among the sites, (F 4,135 = 12.48, P < 0.001, table 5), being

significantly higher for basin plants than for any hybrid or

mountain plants. Mountain plants had the lowest MAD

distances. Similarly, CRDs varied among the sites (F 4,135 =

2.73, P < 0.03, table 5) and were highest for the nearmountain plants and lowest for the middle-hybrid plants.

Transplant Gardens

Elemental Concentrations—MADs based upon elemental concentrations differed significantly among the gardens

(F 2,.210 = 7.195, P < 0.001). The mountain garden had the

lowest MADs, which differed significantly from those in the

Table 3—Analysis of spatial heterogeneity of the insect community

using Euclidean distance measures at the Clear Creek Site.

The MAD examines differences among plants in the number

of insects while the CRD examines differences in the

proportion of individuals contributed by each species. Means

subscripted by the same letter do not differ significantly from

one another at the 0.05 level.

Garden Source MAD CRD

Basin Basin 7.39c 0.16a

Basin Near Basin 12.36d 0.54b

Basin Middle Hybrid 12.41d 0.25a

Basin Near Mountain 13.78d 0.19a

Basin Mountain 15.05d 0.35a

Hybrid Basin 6.31c 0.30a

Hybrid Near Basin 7.10c 0.55b

Hybrid Middle Hybrid 3.09b 0.57b

Hybrid Near Mountain 5.52b 0.25a

Hybrid Mountain 3.07b 0.57b

Mountain Basin 0.67a 1.04c

Mountain Near Basin 0.85a 0.98c

Mountain Middle Hybrid 1.61a 0.58b

Mountain Near Mountain 1.54a 0.98c

Mountain Mountain 0.38a 1.07c

Table 4—Analysis of the spatial heterogeneity of terpenes produced by plants at Salt Creek Canyon. The MAD examines differences

among plants in the quantities of terpenes produced while the CRD examines differences in the proportion of terpenes

produced. Means subscripted by the same letter do not differ at the 0.05 level.

Basin Near basin Middle hybrid Near mountain Mountain χ2 P

MAD 0.41a 0.45a 0.47a 0.87b 0.74b 42.8 0.000001

CRD 1.37 1.37 1.37 1.35 1.34 0.4 N. S.
USDA Forest Service Proceedings RMRS-P-21. 2001 131

Use of Distance Measures to Assess Environmental and Genetic Variability... Freeman, Graham, Jones, Wang, Miglia, and McArthur

basin and hybrid gardens; the MADs for these latter two

gardens did not differ from one another. MADs also differed

significantly among source populations (F 4,210 =3.231, P <

0.013, table 6). The near-basin plants had the largest MADs,

which differed from the MADs of the basin and near-mountain plants, but not the middle-hybrid or mountain plants.

There was no difference among the gardens and the interaction term was not significant. CRDs differed significantly

among the source populations (F 4,210 = 3.955 P < 0.004,

table 6), but not among the gardens. The mean CRD distance

was significantly greater among the mountain plants than

among the basin, near-mountain and middle-hybrid plants.

The mean CRD among near-basin plants was intermediate.

The garden-by-source population interaction was marginally significant (F 8,210 = 1.93, P < 0.058, table 7).

Biological Absorption Coefficients

MADs distances among plants showed the following significant trend: basin garden > middle hybrid garden > mountain

garden (F 2,210 = 27.003, P < 0.001). MADs also varied

Table 5—An analysis of the spatial heterogeneity among plants in concentrations of 10 elements in leaf tissue. The MAD distance examines the

concentrations of the elements; the CRD distance examines the proportions of elements. Both site-indigenous and reciprocally

transplanted individuals were examined. Means subscripted by the same letter do not differ at 0.05 level.

Site-indigenous plants

Elemental concentrations Basin Near basin Middle hybrid Near mountain Mountain F(4,135) P

MAD 526.57a 294.28b 542.72a 400.44ab 312.68b 6.14 0.001

CRD 0.15ab 0.09a 0.18b 0.13ab 0.1a 4.19 0.003

Biological absorption coefficient

MAD 10.14a 6.37b 6.95b 5.71b 3.2c 12.48 0.001

CRD 0.09ab 0.07ab 0.06a 0.10b 0.09ab 2.73 0.03

significantly among the source populations (F 4,210 = 4.001,

P < 0.004, table 6). MADs were greatest among the middle

hybrids, and least among near-mountain hybrids. The other

source populations were intermediate and did not differ

from each other, the middle-hybrid or near-mountain plants.

The interaction among gardens and source populations was

also significant, (F 8,210 = 4.563, P < 0.001, table 6 and fig. 2).

As a general rule, site-indigenous plants had the lowest

MADs, while nonindigenous parental plants and at least one

type of hybrid had the greatest MADs.

CRDs showed the following significant trend: mountain

garden > basin garden > middle-hybrid garden (F 2,210 =

48.070, P < 0.001). CRDs also varied significantly among the

source population (F 4,210 = 9.210, P < 0.000, table 6 and

fig. 2). CRDs were significantly greater for middle hybrid

and basin plants than for mountain and near-mountain

plants. Near-basin plants were intermediate. The interaction between garden and source population was also significant (F 8,210 = 3.420, P < 0.001, table 6). In general, CRDs

were greatest for hybrid and basin plants and lowest for

mountain plants; however, relative ranking among the different hybrid sources varied among the gardens.

Table 6—An analysis of the spatial heterogeneity in the concentrations of elements and the biological absorption coefficients

among plants in the transplant gardens at Salt Creek Canyon. The MAD distance examines heterogeneity in the

concentrations of elements while the CRD distance examines differences in the proportions of the elements.

Source population

Elemental concentration Basin Near basin Middle hybrid Near mountain Mountain

Garden

MAD Basin 560.77a 808.16b 593.87a 533.63a 824.88b

MAD Hybrid 628.41 779.26 711.44 624.7 729.87

MAD Mountain 509.6 629.93 590.22 463.27 426.23

CRD Basin 0.16ab 0.19ab 0.12ab 0.09a 0.21b

CRD Hybrid 0.1a 0.17ab 0.11a 0.18ab 0.22b

CRD Mountain 0.14 0.14 0.16 0.13 0.16

Biological absorption coefficients

MAD Basin 75.42a 100.85ab 81.75a 74a 107b

MAD Hybrid 65.16 48.66 62.56 53.85 47.45

MAD Mountain 59.66a 63.5a 84.71a 25.11b 27.03b

CRD Basin 0.19a 0.13ab 0.15ab 0.09b 0.12ab

CRD Hybrid 0.09 0.07 0.1 0.07 0.05

CRD Mountain 0.2ab 0.26bc 0.31c 0.15a 0.12a
132 USDA Forest Service Proceedings RMRS-P-21. 2001

Freeman, Graham, Jones, Wang, Miglia, and McArthur Use of Distance Measures to Assess Environmental and Genetic Variability...

Figure 2—Comparison of MAD and CRD distances based upon plant chemistry among the five source populations.

Discussion _____________________

Here we examined the potential correlation between the

spatial variability of key ecological parameters across two

big sagebrush hybrid zones, as well as the enhanced genetic

variation conferred by hybridization. Variability in parental

and hybrid plant responses (in terms of secondary chemicals, leaf elemental composition and biological absorption

coefficients) to these ecological gradients were also examined in reciprocal transplant gardens across one hybrid

zone. The results, while complex, nonetheless demonstrate

several important points. First, the hybrid zone occurs at an

ecotone. Prior analysis of the soils demonstrated that soil

chemistry changes abruptly across the hybrid zone and

becomes spatially more variable, particularly in the proportions of elements, within the hybrid zone. The vegetation

goes from a floristically poor community in the basin zone to

a very diverse community in the mountain zone. While the

amount of ground cover is quite variable in the basin community, species composition is remarkably uniform. The reverse is true in the mountain zone. Species composition

changes markedly from quadrat to quadrat, but the amount

of plant cover is relatively uniform. The product of these two

measures shows that the hybrid zone is intermediate for

both trends and is more uniform in both the amount of cover

and species composition than either parental site. The insects found on sagebrush plants follow the same basic trends

as the vegetation. The numbers of insects feeding on plants

in the basin garden varied greatly among the plants, but the

species composition of these insects was quite uniform. In

the mountain garden (where there are considerably more

species), the species composition of insects feeding on big

sagebrush varied considerably from plant to plant, but

insect density was quite uniform. The hybrid zone was

intermediate just as it was with the vegetation. Thus it

appears that the hybrid zone is found in a zone of sharp

ecological transition.

The second major trend involves the reciprocal transplant

gardens. Both insect and leaf chemistry data show variation

among plants from the same source population to be greater

for nonnative plants than those site-indigenous plants. This

trend suggests that nonnative plants are more stressed than

those indigenous to a particular site. This idea is not new;

organisms under stress are known to display greater genetic

variation (see Galaud and others 1993 for an excellent

example). Similarly, insects are well known to prefer

plants under stress (Whitham and others 1994; White

1976; Waring and Cobb 1992; Paige and Capman 1993).

These results are, therefore, easy to understand in light of

well-established patterns.

Basin Near

Basin

Middle

Hybrid

Near

Mountain

Mountain

Elemental Concentrations CRD

0.25

0.2

0.15

0.1

0.05

0

Basin Near

Basin

Middle

Hybrid

Near

Mountain

Mountain

Elemental Concentrations MAD

1000

800

600

400

200

0

Basin Near

Basin

Middle

Hybrid

Near

Mountain

Mountain

Biological Absorption Coefficient CRD

0.25

0.2

0.15

0.1

0.05

0

Basin Near

Basin

Middle

Hybrid

Near

Mountain

Mountain

Biological Absorption Coefficient CRD

0.25

0.2

0.15

0.1

0.05

0
USDA Forest Service Proceedings RMRS-P-21. 2001 133

Use of Distance Measures to Assess Environmental and Genetic Variability... Freeman, Graham, Jones, Wang, Miglia, and McArthur

The third trend is that in the transplant gardens, overall,

hybrids typically display greater plant-to-plant variation

primarily in their biological absorption coefficients, but also

in leaf chemistry. The source population term in the

ANOVA model reflects at least a partial genetic contribution. Our findings that hybrids display greater variability is not surprising. Hybridization is well known to lead to

increased phenotypic variability. This also corresponds well

with our earlier results showing enhanced spatial variation

in the proportions of elements in the soils (Wang and others

1998).

We have repeatedly shown that structuring of the big

sagebrush hybrid zone is due to plant-by-soil interactions.

Microbes are well known to mediate this type of interaction.

A separate study (Miglia and others, in preparation) shows

that the microbial community varies across the hybrid zone,

and that growth of big sagebrush is contingent upon both the

source population from which the plants originated and the

microbial composition of the soils in which the plants were

raised. This may partially explain the boundaries of the

hybrid zone. Within each zone, indigenous plants should be

under directional selection, thereby resulting in their

adaptation to the indigenous microbial community. If this

is true, then hybridization appears to provide the genetic

variation needed to adapt to the more variable and unique

edaphic properties (both biological and chemical) of the

hybrid zone.

References _____________________

Arnold, M. L. 1997 Natural hybridization and evolution. Oxford

University Press, NY.

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of big sagebrush (Artemisia tridentata: Asteraceae). XIV. The

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Subspecies.

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two big sagebrush subspecies (Artemisia tridentatassp. tridentata

and A. t. ssp. vaseyana. Ph.D. dissertation, Wayne State University, Detroit, MI, U.S.A.

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134 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Andrés F. Cibils was Ph.D. Candidate in the Rangeland Ecosystem Science

Department of Colorado State University at the time this study was conducted. He now does rangeland management research at INTA-EEA Santa

Cruz, Casilla 332, (9400) Río Gallegos, Santa Cruz, Argentina. David M. Swift

is a Senior Research Scientist at the Natural Resource Ecology Laboratory

and Associate Professor in the Rangeland Ecosystem Science Department

both at Colorado State University, Fort Collins, CO 80523. Richard H. Hart

is a Senior Range Scientist at the High Plains Grasslands Research Station

of the USDA-ARS, Cheyenne, WY 82009.

Abstract—Previous studies conducted at our research site on the

shortgrass steppe in Colorado showed that phenotypic sex ratios of

tetraploid fourwing saltbush (Atriplex canescens Pursh [Nutt])

shrubs were less female biased in grazed pastures than in adjacent

exclosures. The potential effects of cattle browsing on shrub sex

ratios were studied both in the field and in a greenhouse. In the field

study, winter or late summer grazing resulted in higher utilization

of female shrubs relative to males. In early spring, when shrubs

were browsed the least, utilization of male and female shrubs was

not different. Release from cattle browsing (in temporary exclosures)

was related to sexual phenotype shifts toward femaleness that

occurred mostly in shrubs with monecious phenotypes. Such shifts,

however, did not translate into detectable changes in overall phenotypic shrub sex ratios. In the greenhouse study, female clones of

fourwing saltbush appeared to be more negatively affected by

artificial defoliation than were male or monecious clones. Sex biased

herbivory, and (to a lesser extent) shrub gender specific responses

to defoliation may have promoted higher mortality among female

shrubs possibly leading to shrub sex ratio alteration at this site.

Browsing-induced sex shifts are probably not an important factor

affecting shrub sex ratios at this site.

Introduction ____________________

Sex ratios of dioecious shrubs can change across the

landscape or through time in response to environmental

stress (Freeman and others 1976; McArthur and Freeman

1982; Freeman and others 1993; Allen and Antos 1993).

Gender-specific responses, both to availability of key resources and to a number of biotic and abiotic stressors, are

responsible for such variations (Freeman and others 1980;

Freeman and others 1984). There are at least two basic

processes that can lead to sex ratio alterations, namely:

(a) differential mortality of females and males (Williams and

others 1978); or (b) phenotypic sex shifting in individuals

Phenotypic Sex Ratios of Atriplex

canescens Shrubs in Relation to

Cattle Browsing

Andrés F. Cibils

David M. Swift

Richard H. Hart

with sexually labile genotypes (Freeman and McArthur

1984; McArthur and others 1992). In stands of tetraploid

fourwing saltbush (Atriplex canescens) on the shortgrass

steppe in Colorado, Cibils and others (1997) found that

female fourwing saltbush shrubs were more abundant inside exclosures than in adjacent grazed pastures.

Fourwing saltbush is fairly sensitive to defoliation (Buwai

and Trlica 1977; Benjamin and others 1995). Seasonal rest

periods are required to keep browsed populations viable

(Pieper and Donart 1978; Price and others 1989). Genderbiased herbivory, that is common in a number of dioecious

shrubs including some saltbushes (Atriplex sp.) (Watson

1995 and references therein; Maywald and others 1998;

Maywald 1999), and/or gender-specific responses to browsing, could promote different mortality rates among male and

female fourwing saltbush shrubs. Additionally, since close

to 55 percent of tetraploid fourwing saltbush shrubs carry

sexually labile genotypes and can shift toward maleness

under stress (McArthur and others 1992), browsing could

promote sex phenotype shifts in fourwing saltbush stands.

Both these processes, potentially driven by cattle browsing,

could be responsible for the sex ratio differences found by

Cibils and others (1997) between exclosures and grazed

pastures.

The objective of our work was to investigate whether cattle

browsing could trigger processes that lead to sex ratio

alterations. We addressed the following questions in a field

and greenhouse study: (1) are female fourwing saltbush

shrubs at our site browsed more intensely than are male

shrubs? (2) does cattle browsing promote sex phenotype

shifts toward maleness in fourwing saltbush at our site?

and (3) are clones from female fourwing saltbush shrubs

affected more negatively by defoliation than are clones from

male or monecious shrubs?

Materials and Methods ___________

Field Study

We conducted the field study at the USDA-ARS Central

Plains Experimental Range (CPER), approximately 60 km

NE of Fort Collins, Colorado (40° 49' N 107° 47' W) at 1,650 m

elevation. We set up the experiment at a shrub-dominated

site, on a floodplain area with loamy to sandy loam soils.

Fourwing saltbush, blue grama (Bouteloua gracilis [H.B.K.]

Lag. Ex Griffiths), and western wheatgrass (Agropyron

smithii Rydb.) are the dominant plant species at the site

(Liang and others 1989). Mean annual precipitation is
USDA Forest Service Proceedings RMRS-P-21. 2001 135

Phenotypic Sex Ratios of Atriplex canescens Shrubs in Relation to Cattle Browsing Cibils, Swift, and Hart

320 mm, most of which occurs between the months of April

and September.

We set up 14 half hectare experimental pastures in two

blocks of seven pastures each, described in detail by Cibils

(1999). We conducted three 2-year browsing experiments (in

1997 and 1998) that consisted of grazing four pastures with

cattle for a period of 4 days in winter (January), early spring

(April), and late summer (September). Two pastures were

grazed moderately (four animals) and two were grazed

heavily (12 animals). Two of the 14 pastures remained as

exclosures. We tagged 20 female and 20 male shrubs in each

experimental pasture before the onset of the experiments in

1996. In June 1997 we tagged an additional 20 monecious

shrubs in each pasture. Tagged shrubs that had shifted

phenotypic sex expression in 1997 or 1998 were replaced in

order to keep numbers of male, female and monecious

shrubs constant. Shortly before each experiment, we marked

and measured the length of four stems on all tagged shrubs.

We re-measured marked stems immediately after removing

cattle, and thus calculated percent length removed by

browsing. Utilization was expressed as a proportion of biomass removed from each marked stem, derived from length/

mass equations described in detail by Cibils (1999). In June

1997 and 1998 we determined sex constancy on all tagged

shrubs by comparing present and previous season’s sexual

phenotype. We also determined shrub sex ratios in each

experimental pasture by recording phenotypic sex expression on 100 shrubs. To do this, we set up two transects per

pasture and recorded sexual phenotype on the closest adult

shrub to each 3 m interval.

Shrub utilization data from each experiment were analyzed separately using a mixed effects repeated measures

analysis of variance. We studied the effects of shrub gender,

stocking density, year and block (of experimental pastures) on

shrub utilization. Utilization data were arcsin transformed

and the overall level of significance was set at P = 0.05. SAS

(1996) Proc GLM was used for the statistical computations.

Sex change on tagged shrubs was analyzed by grouping

shrubs into one of three categories on the basis of their

current season’s floral phenotype, namely: 1) changing

towards maleness (→❹); 2) changing toward femaleness

(→➁); and 3) constant sexual phenotype expression (constant). Nonflowering shrubs were not included in this

analysis. We used a two-way contingency table to analyze

these results by considering two classes of shrubs, namely:

browsed or protected. We built separate tables for 1997 and

1998 and then related them by using the Cochran-MantelHaenzel test of general association. Level of significance

was set at P = 0.05. SAS (1996) PROC FREQ was used for

the statistical computations.

Sex ratios of experimental pastures were also collapsed

into two groups (browsed or protected), and were compared

to the 35❹:55➁:10[❹➁] tetraploid Atriplex canescens sex

ratio described by McArthur (1977) using χ2 goodness-of-fit

tests. We set the level of significance at P = 0.05 and used

Statgraphics (1994) to perform the statistical computations.

Greenhouse Study

During the fall of 1996 we collected cuttings from 30

fourwing saltbush shrubs (10 female, 10 male, and 10

monecious) at five fairly distant sites within the CPER.

Stem-cutting collection, handling, and rooting techniques

used in this study (described in detail by Cibils 1999) matched

specifications proposed by Wiesner and Johnson (1977) and

McArthur and others (1984). Overall, close to 30 percent of

clippings rooted and survived through the first growing season

(1997). We were therefore able to use clones taken from 18

parent fourwing saltbush shrubs in an 8-month experiment

beginning in December 1997, designed to measure the effects

of winter defoliation and water stress on several plant productivity-related variables.

We imposed three defoliation treatments (control, moderate and heavy), and two watering treatments (control and

water stress). The former consisted of one clipping event at

the beginning of the experiment that removed either 40

percent (moderate) or 70 percent (heavy) of the length of all

stems 5 cm or longer. Water stress was imposed by varying

watering intervals. Water in the control pots was replenished when soil water potential reached a value of –1.3

bars. In the water stressed pots, water was replenished

when soil water potential reached a value of –6.5 bars.

The experiment included a total of 108 clones. Treatments

were randomized within parental origin (hereafter referred

to as genotype). Surviving clones did not flower either before

or during the experiment. This frustrated the corroboration

of clone gender by floral phenotype observation. Therefore,

clone gender in this paper must be interpreted as meaning

“clones taken from a donor shrub exhibiting that gender.”

In mid August 1998 we finalized the experiment and

harvested aboveground biomass from all 108 clones, and

root biomass from a subset of 54 clones. Aboveground biomass was harvested, oven-dried and weighed. Roots were

washed and separated from pot soil (using 10 mm, 2 mm, and

1 mm sieves), oven-dried and weighed. In this paper we

discuss the response to the experiment treatments in terms

of total above- and belowground biomass of the subset of

54 clones. Aboveground biomass of defoliated clones included the biomass removed by the clipping treatments

that had been oven-dried and weighed immediately after

defoliation.

We used a mixed effects analysis of variance to analyze

the impact of shrub gender, defoliation regime, watering

regime, and genotype (nested within gender) on total above

and belowground biomass. Significance level was set at

P = 0.05. Means were compared using the LSM method

controlling for comparisonwise error rates. We used SAS

(1996) proc GLM and proc MIXED to perform the statistical

computations.

Results ________________________

Field Study

In January and September percent biomass removed by

cattle from marked leaders on tagged female shrubs was

significantly higher than that removed from male shrubs

(fig. 1). In both of these experiments female-biased browsing

occurred in both years and across a three-fold increase in

cattle density. In April we did not observe any significant

differences in the levels of utilization of male and female

shrubs (fig. 1).

Sex change in tagged shrubs was not significantly associated with browsing when monecious shrubs were excluded
136 USDA Forest Service Proceedings RMRS-P-21. 2001

Cibils, Swift, and Hart Phenotypic Sex Ratios of Atriplex canescens Shrubs in Relation to Cattle Browsing

from the analysis (table 1). However, in 1998 when monecious

shrubs were included, the association was highly significant

(table 1). Whereas sex shifts towards maleness were the

most common, only shifting toward femaleness (that occurred

much more frequently in exclosures) was significantly

associated with cattle browsing (table 1). Shrub sex ratios

in both browsed and protected pastures did not differ

significantly from the 35❹:55➁:10[❹➁] phenotypic frequency, empirically derived for tetraploid fourwing saltbush (McArthur 1977).

Greenhouse Study

Total above- and belowground biomass was significantly

affected by the defoliation-by-gender interaction (F = 2.713;

P = 0.049). Whereas control female, monecious, and male

clones produced similar amounts of total biomass, defoliated

female clones consistently produced less biomass than

clones of the other genders (fig. 2). Under heavy defoliation,

Figure 1—Mean utilization of tagged female (solid

bars) and male (open bars) shrubs in the January, April

and September experiments. F and P values for the

“shrub gender” factor in the repeated measures

ANOVAS are given below each pair of bars. Different

letters indicate significant differences. Comparisons

were made within experiments.

Table 1—Contingency table with counts of shrubs that either changed

sex phenotype or exhibited constant sex phenotype in 1997

and 1998 under cattle browsing or in exclosures.

Shrub counts

Year Treatment →➁ →❹ Constant P

1997 browsed 1 9 90

([❹➁] excluded)

protected 1 13 86 0.672

1998 browsed 1 30 69

(including [❹➁])

protected 13 20 67 0.001**

Overall (C.H.M. Test) 0.001**

Figure 2—Overall means of total above- and belowground biomass for female (solid bars), monecious

(slashed bars), and male (open bars) clones under 3

defoliation levels. Different letters indicate significant

differences. Comparisons were made among genders

within levels of defoliation.

however, differences between males and females were not

statistically significant (fig. 2). Whereas the water stress

treatment we imposed had an overall significant effect on

total above- and belowground biomass (F = 6.846; P = 0.014),

its effect did not depend on the gender of the clone (shrub

gender X water stress: F = 0.886; P = 0.423). It did have,

however, different effects depending on the level of defoliation considered ( water stress X defoliation: F = 5.455; P =

0.01). Water-stressed non defoliated clones produced less

than the controls, however such differences disappeared

with defoliation. We found a considerable amount of genotypic variation within genders (F = 2.332; P = 0.057).

Discussion and Conclusions ______

In January and September female shrubs were browsed

more heavily than were males. In April, when overall shrub

utilization was lowest, we detected no gender bias in utilization. Our results are only partially consistent with sheepbrowsing patterns observed by Maywald and others (1998)

in a fourwing saltbush transplant garden. Sheep preferred

to browse male fourwing saltbush shrubs in June, and

showed no gender-related preferences in March, a date that

is comparable to our April experiment. While we did not find

any instances of significant male-biased browsing, patterns

involving greater use of males relative to females did occur

in some plots of the April experiment in 1997. Our results

tend to match the pattern observed in sheep browsing

bladder saltbush (Atriplex vesicaria Heward ex Benth).

Sheep preferentially browsed female shrubs irrespective of

season and phenological stage (Maywald 1998). In bladder

saltbush stands, female-biased herbivory by sheep is thought

to cause greater mortality among female shrubs thus altering

overall shrub sex ratios (Williams and others 1978). This

may also be the case in the stands of fourwing saltbush that
USDA Forest Service Proceedings RMRS-P-21. 2001 137

Phenotypic Sex Ratios of Atriplex canescens Shrubs in Relation to Cattle Browsing Cibils, Swift, and Hart

we studied. In a previous study of crown and stem dimensions of browsed and protected fourwing saltbush shrubs at

this site, Cibils (1999) found that whereas female shrubs

were apparently younger than males under grazing, in

exclosures such apparent age differences were absent. The

gender-biased browsing pattern we observed could be causing higher mortality of female shrubs at our site as well. This

could ultimately lead to situations of sex ratio alterations.

Experimental pastures that were protected from cattle

browsing exhibited a larger number of tagged shrubs that

shifted toward femaleness than did the pastures that were

browsed. If browsing is in fact a source of considerable stress

to fourwing saltbush shrubs, then our results are consistent

with the trend described by McArthur and Freeman (1982).

In that study, release from stress caused labile shrubs that

had previously shifted toward male sex expression under

stress to return to female flowering status. However, sex

phenotype shifts observed at the level of tagged shrubs did

not translate into detectable deviations of overall shrub sex

ratios at the level of experimental pastures. Labile shrubs

may have been over-represented in our sample of tagged

shrubs. This could account for the apparent lack of consistency between results obtained at the level of tagged individuals and the level of experimental pastures. Browsinginduced sex shifting may not be an important source of sex

ratio alteration in fourwing saltbush stands at our site.

Defoliated female clones produced less above- and

belowground biomass than either male or monecious clones.

Whereas defoliation experiments conducted with dioecious

species have not shown a consistent pattern of genderspecific response (Elmqvist and Gardfjell 1988; Oyama and

Mendoza 1990; Delph and others 1993) female plants are

generally assumed to grow more slowly than their male

counterparts (Jing and Coley 1990). Should this be the case

with fourwing saltbush, it is reasonable to speculate that

female clones were not able to compensate the biomass removed by clipping in a growing season. This could explain

differences in biomass production between genders observed in

our greenhouse experiments. Our results suggest that defoliation may put female shrubs at a competitive disadvantage.

Overall, differences in sex ratios between exclosures and

adjacent grazed pastures at our site reported by Cibils and

others (1997) may have been the result of greater mortality

rates in female shrubs. Both female-biased browsing by

cattle, and possibly higher susceptibility to defoliation in

female fourwing saltbush shrubs may have promoted differences in mortality rates of males and females. Browsingtriggered sex phenotype shifts of labile shrubs are possibly

not important in driving alterations in phenotypic sex

ratios of fourwing saltbush at our site.

Acknowledgments ______________

This work was funded by the United States Department of

Agriculture Agricultural Research Service, High Plains

Grasslands Research Station, Cheyenne, WY. Personal

support for Andrés Cibils was provided by the Instituto Nacional

de Tecnología Agropecuaria, Argentina. The Natural Resource

Ecology Laboratory and the Rangeland Ecosystem Science

Department of Colorado State University provided important logistics support.

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In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Simon A. Lei is a Biology and Ecology Professor at the Community College

of Southern Nevada, 6375 West Charleston Boulevard, WDB, Las Vegas, NV

89146-1139.

Abstract—Plant species with limited dispersal ability, narrow

geographical and physiological tolerance ranges, as well as with

specific habitat and ecological requirements are likely to be rare.

Small and isolated populations and species contain low levels of

within-population genetic variation in many plant species. The

gene pool of plants is a product of phenotype-environment interaction. The effects of inbreeding mating systems, geographical

ecotypes, phenotypic plasticity, microhabitat differentiation, and

stochasticity on genetic variability in locally rare plants are considered. The emphasis of this review paper is on recapitulation of

original data and conclusions of results from a variety of research

studies that approach locally rare plants from ecological and population genetics perspectives.

Introduction ____________________

Temporal and spatial variations in plant population sizes

are detected both within and among species. Some plant

species occur in wide ranges (cosmopolitan), while others are

restricted to only a specific habitat (endemic). This variability is the result of complex interactions among the life

history features of populations, local environmental conditions, and ecological and physiological requirements of particular species (Barnett and Kohn 1991). One often assumes

that rare and endangered species occur in small populations

that are geographically isolated from one another. Rare

plants may be locally common but occur in only a few places

because their habitat is geographically restricted

(Kruckeberg and Rabinowitz 1985). Rare plants may be

locally scarce but geographically widespread. They may also

be both scarce and geographically restricted, reflecting specific adaptation to habitats that are rare (Rabinowitz 1981).

The ecological and evolutionary processes that give rise to

rarity are so complex that one cannot assume all locally rare

plants exhibit the same patterns (Kruckeberg and Rabinowitz

1985). Likewise, some locally rare plants appear to be

genetically depauperate due to their relatively small population size. It may be premature to assume that this is a

universal feature of all locally rare species (Stebbins 1980;

Griggs and Jain 1983).

The distribution and amounts of genetic diversity within

and among populations of locally rare plants depend on

whether a species is naturally rare or whether it has

Ecological and Population Genetics

of Locally Rare Plants: A Review

Simon A. Lei

recently become rare as a result of stochastic events. Stochastic events may be environmental or anthropogenic.

Plant populations that are naturally small may show genetic systems adjusted to close inbreeding, as well as adaptations that offset the disadvantage of rarity, as opposed to

species that have experienced severe reductions in population numbers owing to habitat destruction, fragmentation,

or degradation through anthropogenic activities (Barnett

and Kohn 1991).

The role of ecological and population genetics in locally

rare plants has been increasingly appreciated in recent

years. This paper reviews and discusses some of the genetic

and evolutionary consequences of small population size and

the ecological significance of genetic diversity in locally rare

plants.

Genetic Consequences of Mating in

Small Populations _______________

Differences in survivorship are detected between progeny from selfed and outbred matings within a population

(Barnett and Kohn 1991). They (1991) further state that

some plant species are capable of exhibiting both cleistogamous and chasmogamous flowers. Outcrossed offspring are

expected to be more genetically diverse than the progeny of

self-fertilization. A significant reduction in survivorship is

found for selfed progeny in normally outcrossed plants

(Schoen 1982). Similarly, differences in the relative fitness

of sexually produced offspring versus vegetative (asexually)

produced progeny have also been observed. An intense

exploitation and interference competition would favor sexual

offspring (Case and Taper 1986). Under changing environment, the competitive advantage obtained by the occasional

rare genotype would give the sexual groups competitive

dominance over the asexual (genetically identical) group,

despite the initial advantages of asexual reproduction

(Case and Taper 1986).

Heterozygosity seems to have a fitness advantage, and is

often affiliated with increased growth rates and survivorship in many plant species. Although heterozygosity may not

be advantageous with superior performance when environmental conditions remain relatively stable, heterozygosity

may provide the ability to cope with fluctuating environments, and may play such a buffering role (Grant 1981).

Genetic Variation ________________

Inbreeding

The frequency and intensity of inbreeding are often far

greater in plants than in most animal groups. Unlike most
140 USDA Forest Service Proceedings RMRS-P-21. 2001

Lei Ecological and Population Genetics of Locally Rare Plants: A Review

animals, mature plants are sessile organisms. Seeds, pollen,

and vegetative dispersal structures (for example, rhizome

and stolon) are the only motile stages in the life cycle of a

higher vascular plant. Because of limited gene flow through

pollen and seeds, offspring plants usually germinate and

establish fairly close to the parent, creating small neighborhood sizes. Populations structured into small neighborhoods

appear to be inbred and contain low levels of within-population genetic variation compared to those in larger neighborhoods (Barnett and Kohn 1991). The level of inbreeding in a

plant population increases over time at a rate dependent on

the effective population size, and populations become inbred

more rapidly when they are small in size (Barnett and Kohn

1991).

In plant breeding, it is often useful to know how rapidly

the inbreeding coefficient increases when propagating by a

regular system of mating, such as repeated self-fertilization,

sib mating, and half-sib mating (Hartl 1988). Among the

three mating systems, self-fertilization leads to an extremely

rapidly increase in the inbreeding coefficient (fig. 1). As

expected of highly self-fertilizing species, each individual

plant is highly homozygous for alleles (Hartl 1988). Some

population geneticists propose that self-fertilizing in locally

rare species contain fewer deleterious recessives than do

outcrossing species, presumably because the increased

homozygosity permits harmful recessives to be eliminated

from the population by natural selection (Hartl 1988).

Alternatively, other population geneticists argue that the

potential consequences of inbreeding in locally rare species

include a significant reduction in genetic variability (decreased heterozygosity) and a significant increase in the

frequency of lethal or highly deleterious recessive alleles.

Mating patterns are prime determinants of the levels of

inbreeding in both large and small plant populations

(Barnett and Kohn 1991). In an outcrossing population,

these are maintained by the balance between mutation and

selection. Nevertheless, when an individual self-fertilizes or

inbreeds with a relative, these alleles are often homozygous,

resulting in inbreeding depression (Barnett and Kohn 1991).

Plant populations with a long history of inbreeding due to

specific adaptations to selfing, leading to small population

sizes, would be expected to show a relatively little inbreeding

depression (Templeton and Read 1984). In theory, inbreeding depression usually occurs in normally outcrossing plants, leading to a substantially lower yield and

relative fitness (fig. 2). Conversely, inbreeding depression is

less severe in species that are partially self-fertilizing, and

may be absent altogether in species that are highly selfed

(Wright 1977). In some cases, plant species may be adapted

to further inbreeding (Huenneke 1991). Alternatively, inbreeding depression may occur even in species with a history

of selfing or inbreeding (fig. 3), yet is difficult to accurately

determine the level of inbreeding that a species is likely to

suffer or sustain.

Although plants growing under optimal conditions in a

greenhouse or botanical garden tend to show little or no

inbreeding depression, the effects of inbreeding depression

may be more severe when seeds are released back into the

wild. Seeds produced under uncompetitive conditions may

have relatively low “ecological value,” and small samples of

locally rare plants maintained in botanical gardens may be

inbred and of inferior genetic quality (Barnett and Kohn

1991). For this reason, conservation of wild plants growing in

greenhouses or botanical gardens may lead to unintentional

Figure 1—Theoretical increase in inbreeding coefficient

F for regular systems of mating: selfing, sib mating, and

half-sibing mating (redrawn from Hartl 1988).

0.0

0.2

0 4 8 12 16 20

0.4

0.6

0.8

1.0

Sib mating

Selfing

Half-sib mating

Inbreeding coefficient

Generations

0.0

0.2

1 2 4 8 9

0.4

0.6

0.8

1.0

Yield and relative fitness

Generations of inbreeding (self-pollination)

3 5 6 7

Figure 2—Characteristic loss of yield and relative

fitness associated with inbreeding in a normally crosspollinated plant species. This phenomenon of yield

and relative fitness loss typically occurs with each

successive generation of inbreeding (redrawn from

Kaufmann 1989).
USDA Forest Service Proceedings RMRS-P-21. 2001 141

Ecological and Population Genetics of Locally Rare Plants: A Review Lei

“domestication,” particularly if many sexual generations under optimal conditions are allowed to occur (Barnett and Kohn

1991) at the expense of losing some genetic diversity.

Geographical Ecotypes

Plant species occupying a wide geographical range are

frequently associated with environmental and ecological

conditions. In general, plant species with a wide geographical or ecological range exhibit considerable genetic heterogeneity and phenotypic plasticity (Jain 1979).

Distinct ecotypic variations in growth form have been

observed in plants that are geographically widespread. Distinct ecotypes presumably represent discontinuous genetic

variation, relating to specific habitats. Local ecotypes, varying in morphology or physiology with environmental conditions, reflect genetic differences among populations

(Huenneke 1991). Each plant population is a unique realization of the phenotype-environment interaction (Schwaegerle

and Bazzaz 1987). In many plant populations, ecological

performance associated with genetic differences exists;

such differences are often responses to unusual edaphic,

climatic, geomorphic, or other specific ecological conditions

(Huenneke 1991). For instance, metal tolerance ecotype is

ubiquitous in mine populations, but is nearly absent in

adjacent populations growing on non-mine soils. Despite

some gene flow across the abrupt environmental boundary,

ecotypic variation is maintained by natural selection

(McNeilly and Bradshaw 1968). In general, plants would

have lower growth rate and survivorship than their “resident” ecotypes if they were transplanted to considerably

different environments (Huenneke 1991). Hence, genetic

differentiation among and within populations is frequently

tied to variation in environmental factors, as well as to

geographical and ecological ranges.

Response to Microhabitat Differentiation

Plants experience fine-scale microhabitat differentiations.

Environmental variation influences population parameters,

such as rates of mortality, growth, and reproductive output

among individuals and among populations (Huenneke 1991).

Microsite variation acts to buffer populations from environmental stochasticity, and is especially important for seeds,

seedlings, and small plants (Huenneke 1991).

Some seedlings establishing several meters from their

parent plant may have lower mortality and more rapid

growth than seedlings establishing only 50 m from the parent

(Huenneke 1991). Genetic variability may allow more efficient exploitation of a heterogeneous and changeable environments than would be possible for a genetically uniform

population. However, not all plant species can utilize multiple microsite types efficiently and be buffered from environmental stochasticity. Such multiple microsite types

require a higher genetic variation or phenotypic plasticity.

Response to Stochasticity

Stochastic occurrences play a vital role in determining the

viability of small plant populations. These occurrences may

be genetic or environmental. In general, great heterozygosity characterizes species establishing in variable environments (Beardmore 1983; Loveless and Hamrick 1984; Brown

and Burdon 1987).

Genetic uniformity of a plant population may make the

population highly susceptible to negative biotic interactions, such as herbivory and invasion by insects, pathogens,

parasites, and exotic species. Populations may maintain

genetic polymorphism in defense against biological invasions (Bremermann 1980). Variation in resistance to particular herbivores, pathogens, parasites (biological invasions) appears to be an important evolutionary response to

promote genetic variation. The existence of a range of genotypes in a population may result in the survival of a few

individuals after insect or pathogen attack (Bremermann

1980). The presence of genes for resistance or tolerance

within a population may determine the chance of persistence in the face of insect outbreaks or other herbivory

episodes (Bremermann 1980).

However, some stochastic events act on members of a

plant population regardless of their genetic composition.

Major catastrophic disturbances, such as fire, tornado, hurricane, typhoon, avalanche, landslide, earthquake, tsunami,

and volcanic eruption, may be devastating to all genotypes

in the population. Nevertheless, if disturbances are more

moderate in intensity, genetic variability may lead to the

survival of at least a few individuals in the population

(Huenneke 1991).

Phenotypic Plasticity ____________

A clear distinction between genetic variation and phenotypic plasticity of plants in nature are often difficult to

Figure 3—Relationships between inbreeding depression and the selfing rate assuming lethal or highly

deleterious recessive alleles in a normally cross-pollinated plant species (redrawn from Barrett and Kohn

1991).

0.0

0.2

0.0 0.2 0.4 1.0

0.4

0.6

0.8

1.0

Relative inbreeding depression

Selfing rate

0.6 0.8
142 USDA Forest Service Proceedings RMRS-P-21. 2001

Lei Ecological and Population Genetics of Locally Rare Plants: A Review

determine. Plasticity allows a single genotype to succeed in

a range of environments, and may conceal the true extent of

genetic differentiation (Huenneke 1991). Plasticity has a

genetic basis that varies among individuals and among

populations (Huenneke 1991). Perhaps as a consequence of

being restricted to microsites, plants have evolved remarkable levels of phenotypic plasticity (Schlichting 1986).

Plasticity presumably buffers populations from stochastic

environmental conditions and enhances population viability. Patterns of phenotypic plasticity in individual species

appear to have adaptative significance, and plasticity can be

responsible for a significant amount of life-history diversity and is often a vital product of life-history evolution

(Real 1994). Phenotypic plasticity accounts for some of

the natural variation in life history, but the site-origin

interactions indicate an extensive array of genetic variation in the actual sensitivity and response to environmental

effects (Real 1994).

Although phenotypic plasticity with little genetic heterogeneity would retard the rate of evolution, abundant plasticity has permitted successful germination and establishment

of many plants whose principal mode of reproduction is

vegetative (clonal) propagation. Whether phenotypic plasticity can fully compensate for low genetic variability of a

plant species establishing in a heterogeneous environment

is difficult to determine. However, when a species does not

possess phenotypic plasticity or when a species periodically

experiences environmental stochasticity, genetic variation

can promote population viability.

General Conclusions and Ecological

Implications ____________________

It is imperative to determine to what extent local plant

populations are genetically differentiated, whether such

differences have adaptive value, and whether the mixing of

gene pools from different populations would increase or

decrease successful establishment and long-term survival.

Most plant populations are genetically differentiated from

one another. However, population ecologists and geneticists

are unable to make accurate predictions on whether such

differences would be of adaptive value in the face of changing

environments, or how new genetic combinations are likely to

fare in nature.

Acknowledgments ______________

I gratefully acknowledge David Charlet for providing

critical review on the earlier version of this manuscript.

References _____________________

Barnett, S. C.; J. R. Kohn. 1991. Genetic and evolutionary consequences of small population size in plants. In: Falk, D. A.;

Holsinger, K. E., eds. Genetic and Conservation of Rare Plants.

New York: Oxford University Press. 283 p.

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In: Schoenwald-Cox, C. M.; Chambers, S. M.; MacBryde, B.;

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Bremermann, H. J. 1980. Sex and polymorphism as strategies in

host-pathogen interactions. Journal of Theoretical Biology 87:

671–702.

Brown, A. H. D.; Burdon, J. J. 1987. Mating systems and colonizing

success in plants. In: Gray, A. J.; Crawley, M. J.; Edwards, P. J.,

eds. Colonization, succession and stability. Oxford, U.K.: Blackwell

Scientific: 115–131.

Case, T. J.; Taper, M. L. 1986. On the coexistence and coevolution of

asexual and sexual competitors. Evolution 40: 366–387.

Grant, V. 1981. Plant Speciation, 2nd ed. New York: Columbia

University Press.

Griggs, F. T.; Jain, S. K. 1983. Conservation of vernal pool plants in

California, II. Population biology of a rare and unique grass genus

Orcuttia. Biological Conservation 27: 171–193.

Hartl, D. L. 1988. Population genetics, 2nd ed. Sunderland, MA:

Sinauer Associations, Inc.

Huenneke, L. F. 1991. Ecological implications of genetic variation in

plant populations. In: Falk, D. A.; Holsinger, K. E., eds. Genetic

and Conservation of Rare Plants. New York: Oxford University

Press. 283 p.

Jain, S. 1979. Adaptive strategies, polymorphism, plasticity, and

homeostasis. In: Solbrig, T.; Jain, S.; Johnson, G. B.; Raven,

P. H., eds. Topics in plant population biology. New York: Columbia

University Press: 160–187.

Kruckeberg, A. R.; Rabinowitz, D. 1985. Biological aspects of

endemism in higher plants. Annual Review of Ecology and

Systematics 16: 447–479.

Loveless, M. P.; Hamrick, J. L. 1984. Ecological determinants of

genetic structure in plant populations. Annual Review of Ecology

and Systematics 15: 65–95.

McNeilly, T.; Bradshaw, A. D. 1968. Evolutionary process in populations of coper tolerant Agrostis tenuis. Evolution 22: 108–118.

Rabinowitz, D. 1981. Seven forms of rarity. In: Synge, H., ed.

Biological Aspects of Rare Plant Conservation. New York: John

Wiley and Sons: 205–218.

Real, L. A., ed. 1994. Ecological genetics. Princeton, NJ: Princeton

University Press. 238 p.

Schlichting, C. D. 1986. The evolution of phenotypic plasticity in

plants. Annual Review of Ecology and Systematics 17: 667–693.

Schoen, D. J. 1982. The breeding system of Gilia achilleifolia:

variation in floral characteristics and outcrossing rate. Evolution

36: 352–370.

Schwaegerle, K. E.; Bazzaz, F. A. 1987. Differentiation among nine

populations of Phlox: response to environmental gradients. Ecology 68: 54–64.

Stebbins, G. L. 1980. Rarity of plant species: A synthetic viewpoint.

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Templeton, A. R.; Read, B. 1984. Factors eliminating inbreeding

depression in a captive herd of Speke’s Gazelle. Zoological Biology

3: 177–199.

Wright, S. 1977. Evolution and the genetics of populations, Vol. 3:

Experimental Results and Evolutionary Deductions. Chicago, IL:

University of Chicago Press.
USDA Forest Service Proceedings RMRS-P-21. 2001 143

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

L. St. John is a Plant Materials Center Team Leader and P. Blaker is an

Administrative Assistant, United States Department of Agriculture, Natural

Resources Conservation Service, Plant Materials Center, P.O. Box 296,

Aberdeen, ID 83210.

Abstract—The Plant Materials Center at Aberdeen, Idaho, is

operated by the United States Department of Agriculture, Natural

Resources Conservation Service. The purpose of the Plant Materials Center is to evaluate and release plant materials for conservation use and to develop and transfer new technology for the

establishment and management of plants. The Center serves

portions of Nevada, Utah, California, Oregon and Idaho. ‘Rush’

intermediate wheatgrass was released in 1994 and was chosen for

superior seedling emergence, high forage production and drought

tolerance. In 1995, two selected ecotypes of penstemon were

released. The Richfield Selection of firecracker penstemon has

bright red flowers on upright racemes. The Clearwater Selection

of alpine penstemon has bright lavender flowers on narrow panicles.

Native penstemons provide soil stabilization, plant diversity and

beautification. ‘Bannock’ thickspike wheatgrass was released in

1995 to be used as a component of seed mixes for rangeland and

pasture seedings. The Aberdeen Selection of Laurel willow was

released in 1997. The original material was collected in the upper

Midwest from naturalized stands. The medium to tall shrub has

lustrous, dark green foliage and is very attractive. It shows great

promise for use throughout the Intermountain West in irrigated

windbreaks and as an ornamental.

The Plant Materials Center (PMC) at Aberdeen, Idaho, is

part of the national plant materials program operated by

the United States Department of Agriculture, Natural Resources Conservation Service. The purpose of the plant

materials program is to develop and transfer new technology

for the establishment, use and management of plants.

Plant Materials Centers assemble, evaluate and release

plant materials for conservation use. The Aberdeen PMC

was established in 1939 and has been the primary breeder

and releasing organization for 15 cultivars and 27 alternative releases, and has cooperated in the release of 12

additional cultivars. The Aberdeen PMC serves portions of

Nevada, Utah, California, Oregon, and Idaho. The PMC

works cooperatively with private landowners as well as

State and Federal land management agencies. The PMC

Farm is owned by the South Bingham Soil Conservation

District and is leased to the PMC.

In 1995, the PMC in cooperation with the Idaho Agricultural Experiment Station released two selected ecotypes of

New Plant Releases From the USDA-NRCS

Aberdeen, Idaho, Plant Materials Center

L. St. John

P. Blaker

Penstemon. Except for one minor species, the genus Penstemon does not occur naturally outside of North America.

There are approximately 150 species and most are found in

the Western United States. Penstemons are perennial plants

with opposite leaves, and usually showy, often two-lipped

flowers. The conservation value of these penstemons is soil

stabilization, plant diversity, and beautification of many

different sites. The two penstemons were selected from a

collection of 119 penstemons that were evaluated at the

PMC from 1981 to 1985. They were chosen for their natural

beauty, hardiness and seed production.

The “Richfield Selection” of Firecracker penstemon

(Penstemon eatonii) was collected near Richfield, Utah. Its

natural habitat is the sagebrush, juniper, and ponderosa

pine zones at 3,000 to 8,000 ft (914 to 2,438 m) elevation and

an annual precipitation zone from 10 to 16 in (254 to 406 mm).

It is best adapted to loamy, well-drained soils and can

survive full sunlight, but will not tolerate hot, dry areas. It

is not adapted to areas with poor drainage. Firecracker

penstemon is a perennial, cool-season forb with a fibrous

root system and the stems are often decumbent or reclining.

The leaves are large and slightly pubescent. The flowers are

bright red on upright racemes 24 to 36 in (60 to 91 cm) tall.

The “Clearwater Selection” of alpine penstemon (Penstemon venustus) was collected near the Dworshak Reservoir

on the Clearwater River in northern Idaho. Its natural

habitat is at elevations of 1,000 to 6,000 ft (305 to 1,829 m)

and an annual precipitation zone from 20 to 35+ inches (508

to 889+ mm). Alpine penstemon is best adapted to loamy,

well-drained soils and can survive full sunlight on open,

rocky slopes, but does not do well in areas with poor drainage. It is a perennial, cool-season forb, 12 to 24 inches (30 to

60 cm) tall with a strong taproot and woody base. The leaves

are oblong and sharply serrate. The flowers are bright

lavender to purple-violet and appear in one or more narrow

terminal panicles 12 to 20 inches (30 to 51 cm) long.

The PMC and the Idaho Agricultural Experiment Station

released ‘Rush’ intermediate wheatgrass (Elytrigia

intermedia) in 1994. Rush was selected from a collection

received from the German Botanical Garden, Berlin, in

1962. It was chosen for superior seedling emergence, seedling vigor, high forage production and drought tolerance.

The reason for naming it Rush is because after planting,

seedlings tend to emerge from the soil 3 to 5 days earlier and

in greater numbers than other currently released varieties

of intermediate wheatgrass. Rush has been compared to

many other varieties of intermediate wheatgrass at multiple

locations. It was evaluated for emergence, seedling vigor,

forage production, and drought tolerance.

Rush was found to be superior or equal in all of these

factors on sites with annual precipitation of 12 inches
144 USDA Forest Service Proceedings RMRS-P-21. 2001

St. John and Blaker New Plant Releases From the USDA-NRCS Aberdeen, Idaho, Plant Materials Center

(300 mm) or more. Rush is moderately rhizomatous and

densely tillering, with abundant stems and wide leaves.

Seed is large, averaging 66,000 seeds per pound as compared

to other intermediate wheatgrass varieties which average

80,000 to 90,000 seeds per pound. It prefers well-drained,

loamy to clay textured soils.

Rush can be used to solve a wide variety of conservation

problems including erosion control, forage and cover on sites

receiving 12 to 20 inches (300 to 500 mm) annual precipitation. Rush is protected by Plant Variety Protection (PVP) so

that seed can be marketed only as a class of certified seed.

This will help protect and maintain the characteristics for

which it was released.

The PMC and the Idaho Agricultural Experiment Station

cooperatively released ‘Bannock’ thickspike wheatgrass

(Elymus lanceolatus ssp. lanceolatus) in 1995. Bannock is a

composite of six seed collections from Washington, Oregon

and southeast Idaho. The best performing plants were

selected, isolated and increased to create Bannock. The

grass was developed to be used as a component of a seed mix

for rangeland and pasture seedings. Bannock is especially

adapted to sandy areas with a minimum of 6 inches (152 mm)

annual precipitation. It also provides wildlife cover and

nesting.

Bannock has been thoroughly tested and compared to

other varieties of thickspike wheatgrass in the Western

United States. It was named in honor of the Bannock Indian

Tribe that inhabited the Great Basin. Bannock is a long

lived, leafy, rhizomatous, vigorous, sod-producing, cool season

grass. Thickspike wheatgrass is native to most of the

Northern and Western United States and southern Canada.

The PMC has applied for PVP for Bannock so that seed can

be marketed only as a class of certified seed. This will help

protect and maintain the characteristics for which it was

released.

The “Aberdeen Selection” of Laurel willow (Salix pentandra) was cooperatively released by the PMC and the Idaho

Agricultural Experiment Station in 1997. The original plant

material was obtained from the Rose Lake Plant Materials

Center in Michigan. It was collected in the upper Midwest

from naturalized stands. Laurel willow is native to central

and western Europe where it has been cultivated for many

centuries. The Aberdeen Selection was made from a collection

of potential windbreak plants evaluated at the PMC from

1981 through 1996. This plant was also tested at locations

near Mountain Home, Idaho, and Winnemucca, Nevada. It

shows great promise for use throughout the Intermountain

West in irrigated windbreaks and as an ornamental.

Laurel willow has lustrous, dark green foliage. The shiny

leaves are 2 to 5 inches (5 to 13 cm) long and very attractive.

The bark on the young twigs is green to yellow green and

gray on older branches. It requires deep, moist soils or

supplemental irrigation. The medium to tall shrub has a

dense round top, and symmetrical crown. It has multiple

trunks and grows to heights of 20 to 40 ft (6 to 12 m) with

average canopy coverage of 15 to 25 ft (4 to 8 m). Since it is

an introduced plant from Europe, it is not an appropriate

component for use in natural riparian or wetland areas.
USDA Forest Service Proceedings RMRS-P-21. 2001 4

Disturbance Ecology

and Biodiversity

145

USDA Forest Service Proceedings RMRS-P-21. 2001 147

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Jayne Belnap is an Ecologist and Susan L. Phillips a Biologist, Biological

Research Division, United States Geological Service, 2290 Resource Blvd.,

Moab, UT 84532. Richard Reynolds and Marith Reheis are Geologists, United

States Geological Service, MS 980, Denver, CO 80225. jayne_belnap@usgs.gov

What Makes the Desert Bloom?

Contribution of Dust and Crusts

to Soil Fertility on the Colorado Plateau

Jayne Belnap

Richard Reynolds

Marith Reheis

Susan L. Phillips

Abstract—Eolian dust (windblown silt and clay) and biological soil

crusts are both important to ecosystem functioning of arid lands.

Dust furnishes essential nutrients, influences hydrology, contributes to soil formation, and renders surfaces vulnerable to erosion.

Biological soil crusts contribute directly to soil fertility by fixing

carbon and nitrogen, and indirectly by trapping newly-deposited

dust and stabilizing already-present soil. Results from crust-stabilized, unconsolidated sandy sediments on prominent rock exposures

and grasslands show dust inputs have significantly increased all

bio-essential nutrients in soils of SE Utah, including P, K, Mg, Na,

and Ca. As plants can be P and K-limited in these soils, dust may be

essential for plant growth. Evidence for eolian dust comes from

magnetic, chemical, and mineralogic properties of the soils that

contrast greatly with those of local bedrock. For example, magnetite, which formed originally in igneous rocks, is common in soils but

absent in the local sedimentary bedrock. In view of the regional

geology, particle-size distribution of soils, and patterns of properties, the magnetite represents long-distance transport of eolian

dust. Dust in the biological soil crusts, when compared to underlying

sediment, shows higher magnetite, Zr, and Zr/Ti, suggesting that

dust sources have changed over the past few decades. It is suggested

that recent human disturbance in areas surrounding the Colorado

Plateau may be responsible for this change in dust source. Because

most of the fertility in these soils is due to dust input, it is of concern

to land managers when soil loss via wind and water erosion exceeds

this input. Ever-increasing use of these desert landscapes by recreation, military and agricultural activities generally destroys the

biological soil crusts that are critical for nitrogen, carbon, and soil

stability. Thus, increased erosion, and reduced dust retention, may

be a result of these activities.

Introduction ____________________

The source of desert soil fertility has long been a question

for many scientists. Weathering of soils from parent material in this region is generally very slow, taking 5,000–

10,000 years (Dregne 1983). Rainfall is low, and thus nutrient input via wet deposition is limited. Few nitrogen-fixing

plants are found in these regions (Wullstein 1989), and

sparse vascular vegetation limits carbon inputs. Eolian dust

has recently been demonstrated to be an important source of

nutrients for a wide range of ecosystems (Chadwick and

others 1999). Eolian dust has been identified, primarily on

the basis of chemical, mineralogic, and textural properties,

in several types of surficial deposits in arid environments

(McFadden and McAuliffe 1997; Reheis and others 1995).

However, because such dust is wind-transported, it also

renders the soils and sediment in which it resides vulnerable

to subsequent wind erosion.

Biological soil crusts can contribute to soil fertility in

deserts in many ways. They have high C fixation rates, and

significant amounts of C can be fixed during seasons when

soils remain wet for extended periods (Beymer and Klopatek

1991; Belnap and Lange 2001). Much of the C fixed by crust

organisms is used for extracellular polysaccharide production or leaked into surrounding soils. Because desert microbial populations are generally C-limited (Follett 2001), soil

crusts may be critical in sustaining decomposition in these

soils. Biological soil crusts influence soil temperature, moisture levels, aeration and porosity (Harper and Marble 1988;

Belnap 1995; George and others, unpublished data). Soil

crusts influence vascular plant productivity by being a

dominant source of N (Evans and Ehleringer 1993), mostly

due to N fixation by the soil lichen Collema (Belnap 1996).

Cyanobacteria secrete powerful metal chelators and other

substances that maintain nutrients in plant-available forms

despite the high pH of desert soils (Belnap and Lange 2001).

Crusts are also critical for soil stability and aggregate

formation (Belnap and Gardner 1993; Williams and others

1995a; Belnap and Gillette 1997, 1998).

Most lands in the Western United States, once isolated

and seldom visited, have undergone escalating use since the

late 1800s. Historically, most of the land use was limited to

livestock grazing in areas where free surface water was

available; more recently, substantial increases in recreation, military activities, and agriculture have expanded

human use (both spatially and temporally) of arid and

semiarid regions. The current combination of land use is

leading to unprecedented levels of surface disturbance on

many of these lands. Generally, soil surface disturbance

and/or the invasion of annual grasses results in the loss of

lichens and mosses, leaving cyanobacterial-dominated crusts

(Belnap 1995; Harper and Marble 1988), which is expected
148 USDA Forest Service Proceedings RMRS-P-21. 2001

Belnap, Reynolds, Reheis, and Phillips What Makes the Desert Bloom? Contribution of Dust and Crusts to Soil Fertility on the Colorado Plateau

to alter many aspects of nutrient cycling and soil stabilization (Belnap and Gillette 1998).

This study documents the presence of eolian silt in surficial

sediment on part of the Colorado Plateau. We show how the

biological soil crusts in this region enhance and maintain

soil fertility through C and N fixation, dust trapping, and soil

stabilization. We then discuss how soil surface disturbance

alters this situation.

Sampling and Methods ___________

Dust Inputs

Sediment was collected from potholes on slickrock, mesa

tops, and grassland settings. Bedrock consisted of either red

sandstone, brown to gray sandstone, or limestone. We analyzed sediment both within the biological soil crust and

below to depths of 5 cm. We used a combination of reflectedlight petrographic and magnetic techniques to determine

the amounts, types, and origins of magnetic minerals. Magnetic property measurements included: (1) magnetic susceptibility (MS), a measure of the amount of all magnetic

material but mainly ferromagnetic minerals (such as magnetite) when present; (2) frequency-dependent MS (FDMS;

from measurements at 600 Hz and 6000 Hz), a measure of

the amount of ultrafine grained magnetite, or magnetitelike maghemite, commonly attributed to pedogenic origins;

(3) “hard” isothermal remanent magnetization (HIRM), a

measure of the amount of hematite; and (4) the S parameter

[the ratio of backfield isothermal remanent magnetization

(IRM) at 0.3 Tesla (T) and IRM at 1.2 T], in this setting an

indication of relative amounts of magnetite and hematite.

Trace and minor-element chemistry was determined using energy-dispersive X-ray fluorescence (XRF). Changes in

Fe (commonly mobilized via primary mineral alteration), Ti

(chemically immobile and associated with certain magnetic

Fe oxide minerals), and Zr (also chemically immobile) are

especially useful in evaluating potential post-depositional

alteration of magnetite and possible shifts in sediment sources.

Biological Crust Inputs and Soil Retention

The site of this study was the Needles District of

Canyonlands National Park, located 125 km south of Moab,

UT. Annual rainfall averages 215 mm, with approximately

35 percent falling as summer monsoons. To estimate N

inputs, we used data from a datalogger that has continuously recorded amount and time of rainfall, and air and soil

temperatures, since April 1998. Using this data, we grouped

precipitation events into six temperature categories (–4 to

4 °C, 5–8 °C, 9–17 °C, 18–23 °C, 24–27 °C, and 28–35 °C). We

used a combination of manual dry-down curves and TDR

results (that measured soil moisture in the top 1 cm of soil)

to determine how long 1 mm of precipitation at different

seasons and different air temperatures lasted in study soils

for each temperature category. We then multiplied the

precipitation received at a given temperature by the time

soils took to dry at that temperature to estimate the number

of hours soils are wet. We used a combination of laboratory

and field-obtained N fixation values for each of the temperatures and multiplied this by the number of hours soils were

wet at each temperature (Belnap 2001a). Because crusts are

able to fix 4-6 hours during the dark, 50 percent of the

nighttime hours were considered available for N fixation.

Studies of N fixation utilized the acetylene reduction

technique, which requires conversion to absolute N values

using 15N2 calibration. This was done for soil Nostoc from the

Moab, UT area by Phillips and Belnap (unpublished data);

a conversion ratio of 0.31 was obtained, and is used for

estimates of N inputs. A similar value for the same organism

was measured by Liengen (1999) from arctic soils. It should

be noted that this low conversion ratio gives much higher

values for N inputs than is commonly reported in the

literature. Most of these studies did not do the necessary

experiments to find the appropriate conversion ratio, and so

relied on the theoretical ratio of 3C2H4:1N. However Liengen

showed that this value is only accurate for cultured

cyanobacteria and that for field-collected organisms, a much

lower conversion ratio should be used.

Data from studies previous published (Belnap and Gillette

1997, 1998) and unpublished (Belnap and others) were used

to estimate accelerated soil losses due to conversion of lichen

crusts to cyanobacterial crusts. This data was also used to

estimate losses from wind and water immediately following

surface disturbance on sandy soils.

Results and Discussion __________

Dust Inputs

The MS of the host sedimentary rock was very low at all

sites tested (11 sites, 2.4 x 10–10 to 1.1 x 10–8 m3

/kg). In

contrast, MS values of the surficial sediment were between

one and three orders of magnitude greater than the corresponding site bedrock (site averages, 3.5 x 10–8 to 1.5 x 10–7

m3/kg), with MS at most sites highest in the biological soil

crust (fig. 1a). The S parameter values indicate that there is

a much greater concentration of magnetite relative to hematite in the soil crusts than below the surface (fig. 1b). While

such patterns in MS and S parameters suggest the presence

of eolian dust, they are not sufficient proof, as enhanced MS

in upland soils and sediments (away from alluvial input)

may result from other factors such as pedogenic production

of ultrafine grained iron oxide minerals, concentration of

residual minerals, and bacterially mediated reactions

(Dearing and others 1996). Moreover, diagenetic or pedogenic alteration of magnetite at depth may produce a

pattern of highest MS and S values at the surface.

However, the eolian origin of the observed MS enhancement is supported by other magnetic properties and geochemical results seen in these soils. Hematite content was much

greater in surficial sediment than in the underlying bedrock,

even including hematite-bearing redbeds (fig. 1c), as would

be expected for eolian addition of hematite with magnetite.

Moreover, FDMS values were small, implying pedogenic

iron oxide contributed only a small amount (fig. 1d). Large

differences in elemental content were seen between the

surficial sediment and bedrock (fig. 2). For example, surficial

sediment had higher average contents of Fe (≈1 wt. percent),

Ti (≈0.15 wt. percent), and Zr (≥200 ppm) than local bedrock

(Fe, 0.7 wt. percent; Ti, 0.08 wt. percent; Zr<100 ppm).

Nearly constant Fe/Ti values (fig. 2), along with textural

evidence, indicate a lack of magnetite destruction below the
USDA Forest Service Proceedings RMRS-P-21. 2001 149

What Makes the Desert Bloom? Contribution of Dust and Crusts to Soil Fertility on the Colorado Plateau Belnap, Reynolds, Reheis, and Phillips

biological soil crust. The overall thinness of layers, magnetic

mineralogy, and resistant underlying bedrock preclude

magnetic and elemental enrichment of the surficial layers

by chemical weathering and residual accumulation.

The definitive test for the origin of magnetite and hematite in this setting is petrographic comparison of grains

extracted from the sediment and bedrock. In these sediments, magnetic minerals include mainly silt-sized (5–60 mm)

magnetite and associated oxides, such as ilmenite, hematite, and varieties of other Fe-Ti oxides that result from hightemperature oxidation of magnetite and ilmenite. These

associated minerals, and the internal textures of magnetite

with ilmenite lamellae, indicate that the magnetic Fe-Ti

oxide minerals originated in igneous rocks. Such magnetite

and associated minerals are absent in sandstone at the

sampling sites, although limestone may contain only very

rare magnetite or maghemite formed via oxidation of pyrite.

Combined, this evidence suggests that a major component

of the surficial deposits must be eolian to account for their

high content of strongly magnetic minerals, which are absent or sparse in the underlying bedrock. Moreover, fly-ash

magnetite, produced via coal combustion in power plants, is

observed in the biological soil crust, but has not been found

in the underlying surficial sediment. Silt plus clay content

typically ranges between 20 and 50 percent, implying a

similar range in eolian dust content.

Hematite Magnetite

Magnetite content Hematite content

Ultrafine magnetite content

BSC

D

-6 -4 -2 0 2 4

0

1

2

3

4

5

6

7

BSC

A

0 2 4 6 8 10 12

0

1

2

3

4

5

6

7

BSC

C

0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5

0

1

2

3

4

5

6

7

B

BSC

0.45 0.50 0.55 0.60 0.65

0

1

2

3

4

5

6

7

Depth (cm)

MS (x10 m kg ) -8 3 -1

FDMS (x10 m kg ) -9 3 -1 S parameter

HIRM (x10 Am kg ) -4 2 -1

Depth (cm)

Figure 1—Plots of depth versus magnetic properties, as

averages from sandstone sites. (A) magnetic susceptibility; (B) S parameter; (C) “hard” isothermal remanent

magnetization; (D) frequency-dependent magnetic susceptibility. Uppermost sample represent biologic soil

crust values. Solid pattern represents bedrock values.

Figure 2. Plots of depth vs. zirconium (A); titanium (B);

Zr/Ti (C); Fe/Ti (D). Patterns as in Figure 1.

r;

yBSC biologic soil crust

surfic ial sedim ent or soil

bedrock

BSC

BSC BSC

BSC

B D

0 2 4 6 8 10

0

1

2

3

4

5

6

7

A

0 100 200 300

0

1

2

3

4

5

6

7

C

0.00 0.05 0.10 0.15 0.20

7

0.00 0.05 0.10 0.15

0

1

2

3

4

5

6

7

0

1

2

3

4

5

6

Zirconium (ppm) Zr / Ti

Titanium (wt. %) Fe / Ti

Depth (cm) Depth (cm)

Figure 2—Plots of depth versus zirconium. (A) Titanium; (B) Zr/Ti; (C) Fe/Ti; (D) Patterns as in figure 1.

The biological soil crust, which stabilizes the surficial

material, is a natural dust trap and appears to have documented a change in dust source over the past several decades.

Relative to underlying sediment, this crust layer has higher

magnetite (both absolute and relative to hematite), higher

Zr/Ti, and nearly constant Fe/Ti (fig. 2). These shifts in

magnetic and chemical properties are consistent with increased eolian input from desert regions (much underlain by

granitic and rhyolitic rocks) west and southwest of the

Colorado Plateau. The shifts may also represent more input

from the mildly alkaline intrusive rocks that form the

Henry, Abajo, and La Sal Mountains of the central Colorado

Plateau. Either way, the magnetic and chemical shifts

recorded in the biological soil crusts may reflect recent,

intensive human disturbance of arid lands.

In light of the above evidence, the contribution of dust to

soil fertility in this region is striking. As can be seen in figure

2, the deposition of dust has enhanced most plant-essential

nutrients in these soils. Enriched nutrients include phosphorus (2x), potassium (1.2x), magnesium (4.4x), sodium

(3.8x), calcium (10.5x, except in calcite-cemented sandstone

sites), iron (1.6x), copper (1.4x), manganese (2.1x) and molybdenum (13x). Amounts and distribution patterns of enrichment are similar between sites, and magnesium, sodium,

calcium, copper and zinc are consistently higher in the

biological soil crust relative to underlying sediment.
150 USDA Forest Service Proceedings RMRS-P-21. 2001

Belnap, Reynolds, Reheis, and Phillips What Makes the Desert Bloom? Contribution of Dust and Crusts to Soil Fertility on the Colorado Plateau

Biological Soil Crust Inputs and Soil

Retention

Biological soil crusts have long been known to fix carbon

and nitrogen, and estimates of their annual contributions

have been made by multiple authors (Jeffries and others

1993; Belnap 2001a; Evans and Lange 2001). Beymer and

Klopatek (1991) estimated potential annual C contribution

of lichen soil crusts to be 12–37 gC m–2 year–1. Lange and

others (1994) estimated lichen crusts in Namibia to contribute 32 gC m–2 year–1 lower range. Lower rates have been

reported for cyanobacteria-dominated crusts (0.4–2.3 gC

m–2 year–1; Garcia-Pichel and Belnap 1996). Because short

wet-dry cycles in summer lead to C deficits due to drying of

soils before net photosynthesis can be reached (Jeffries and

others 1993), most C inputs occur during the cooler seasons.

Less is known about N fixation in this region. Our recording datalogger showed that rainfall events were surprisingly common in SE Utah during the measurement period.

Between June 15, 1998, and September 15, 2000, 129 soilwetting events were recorded (intermittent rains during

consecutive days were considered one event if the soils did

not dry between rain showers), an average of 4.8 events each

month. The number of rain events in any given season, and

the amount of rainfall, was highly variable, and within the

2-year measurement period, showed no obvious pattern

among seasons (table 1). The number of rain events at night

relative to those occurring during the day was also highly

variable. Combining these results with average N fixation

rates at a given temperature, we were able to estimate

seasonal and annual N inputs for 2 measured years: 41 kgN/

ha/yr for lichen crusts, and up to 13 kgN/ha/yr for cyanobacterial crusts (depending on biomass of a given crust).

This represents a major input of N to soils of these ecosystems.

All crust components secrete extracellular C within minutes to a few days of C acquisition, and the presence of soilcrust organisms can increase soil polysaccharides and total

carbon by up to 300 percent (Rao and Burns 1990; Rogers

and Burns 1994), benefitting surrounding heterotrophic

microbes which are often carbon limited. In addition, this

input of carbon can lower soil C:N ratios, thus increasing

decomposition rates (Kleiner and Harper 1972).

Up to 70 percent of the nitrogen fixed by cyanobacteria and

cyanolichens is released immediately into the surrounding

soil environment, and is available to associated organisms

including vascular plants, mosses, fungi, and other microbes

(Belnap 2001a). Multiple studies have reported that the

presence of soil crusts increases surrounding soil N by up to

200 percent (Shields and Durrell 1964; Rogers and Burns

1994; DeFalco 1995; Harper and Belnap 2001), and stable

isotopes show soil crusts can be the dominant source of N for

desert soils and plants (Evans and Ehleringer 1993; Evans

and Belnap 1999).

Crusts affect soil nutrients in many other ways as well.

Microbial exopolymers both add carbon to soils as well as

create a mosaic of polyfunctional metal binding sites that

bind both cations and anions (Greene and Darnall 1990),

thus preventing them from leaching from sandy soils. Most

of these polymers also concentrate plant-essential nutrients

such as Na, K, Mg, Ca, Mn, Fe, Ni, Cu, and Zn (Lange 1976;

Geesey and Jang 1990). As they are adsorbed to the extracellular sheath, and are not absorbed by the cells, they remain

available to plants (Geesey and Jang 1990). Cyanobacteria,

green algae, fungi, lichens, and bacteria also secrete powerful metal chelators such as siderochromes (Lange 1974;

McLean and Beveridge 1990; Schelske 1962) that can maintain metals in bio-available forms, and can concentrate

essential trace metals found at exceedingly low ambient

concentrations (Paerl 1988). Cyanobacteria secrete peptide

nitrogen and riboflavin which, together with siderochromes,

keep P, Cu, Zn, Ni, and Fe plant-available. These secreted

chelators are water soluble, and capable of being translocated in soil and water. Consequently, chelated compounds

are made available to associated plants or microbes (Bose

and others 1971; Lange 1974; Geesey and Jang 1990; Gadd

1990a). Cyanobacteria also secrete glycollate, which stimulates the uptake of P in cyanobacteria (Fogg 1966), as well as

various vitamins such as B12, auxin-like substances, and

other substances that promote growth and cell division in

plant and animal tissue (Fogg 1966; Venkataraman and

Neelakantan 1967). Biological crusts are also important in

trapping dust and stabilizing soils. Studies have shown that

the top few mm of soil contain a much higher percentage of

soil fine particles than underlying soils, indicating that

crusts trap and entrain falling dust particles (Danin and

Ganor 1991; Verrecchia and others 1995). Because dust can

be a critical component of soil fertility, as discussed above,

this capture and retention is an essential part of soil building

in deserts.

Over 30 studies worldwide have shown that biological soil

crusts reduce soil loss by wind and water (Belnap 2001b;

Warren 2001a,b). Cyanobacterial and microfungal polysaccharides entrap and bind soil particles together, creating

soil aggregates, which are then further linked together into

larger aggregates (Belnap and Gardner 1993). These larger,

linked aggregates require greater wind and water velocity to

move than single soil particles (Gillette and others 1980;

Marticorena and others 1997). Resistance to erosion increases with biological crust development (Belnap and

Gillette 1998), with cyanobacterial crusts showing the least,

and lichen crusts showing the greatest, resistance to erosive

forces. In most cases, lichen crusts can withstand winds well

above those recorded at field sites, and so offer complete

protection from wind erosion, even in coarse soils (Leys

Table 1—Amount of precipitation (mm) by time of day and

season for 1998–2000. Spring = March 16–June 15;

Summer = June 16–September 15; Fall = September

16–December 15; Winter = December 16–March 15.

Day Night Total

Spring 1999 129 318 447

Spring 2000 162 19 181

Summer 1998 40 49 89

Summer 1999 121 61 183

Summer 2000 8 10 18

Fall 1998 308 271 579

Fall 1999 128 70 199

Winter 1998 183 56 239

Winter 1999 206 146 352
USDA Forest Service Proceedings RMRS-P-21. 2001 151

What Makes the Desert Bloom? Contribution of Dust and Crusts to Soil Fertility on the Colorado Plateau Belnap, Reynolds, Reheis, and Phillips

1990; Williams and others 1995a; Belnap and Gillette 1997,

1998; Leys and Eldridge 1998). Exhaustive field and lab

studies show that increasing crust cover and/or development also significantly reduces sediment loss via water

erosion (Booth 1941; Loope and Gifford 1972; Rushforth and

Brotherson 1982; Brotherson and Rushforth 1983; Harper

and St. Clair 1985; Williams and others 1995b).

Effects of Soil Surface Disturbance

on Soil Fertility

Overall, disturbance generally results in loss of species

diversity, biomass, and surface cover of cyanobacteria, lichens, and mosses. The more severe the disturbance, the

greater the loss. Thus, after severe disturbance, the resulting crust community is greatly simplified from a community

with multiple species of cyanobacteria, lichens, and mosses

to a community often dominated by one or a few species of

cyanobacteria. A shift from a lichen to a cyanobacterialdominated crust will reduce C inputs, as cyanobacteria fix

less C than lichens and mosses per unit soil surface area

(Phillips and Belnap 1998). As discussed above, much of this

C is released into the surrounding soils (Lewin 1956); thus,

reduced C fixation is expected to reduce soil C available for

microbial populations, decomposition rates and soil nutrient

levels (Paul and Clark 1996).

Soil surface disturbance and/or a shift from a lichen to a

cyanobacterial-dominated crust also decreases N inputs.

Our annual input estimates are four times higher for lichen

crusts than cyanobacterial crusts. Laboratory and field

studies have consistently shown that lichen crusts have

higher N fixation rates than cyanobacterial crusts (Jeffries

and others 1993 a,b; Belnap and others 1994; Belnap 1995,

1996; Belnap 2001a). Multiple studies have shown less N

input from crusts following disturbance. Vehicles, human

foot traffic, mountain bikes, and raking reduced N input

from crusts 25-89 percent, with a drop of 80-100 percent over

time due to subsequent death of buried material (Belnap and

others 1994; Belnap 1995, 1996). Grazing reduces N inputs

by 50-95 percent (Brotherson and others 1983; Johansen

and St. Clair 1986; Jeffries and others 1992; Terry and

Burns 1987). Burning can reduce N inputs by 64 percent and

tilling by 99 percent (Terry and Burns 1987). Evans and

Belnap (1999) showed N fixation was still 2.5 times less than

an adjacent, never-grazed area 30 years after grazing had

ceased. Decreased N inputs from crusts can have long-term

impacts on soil N levels. On the Colorado Plateau, Jeffries

(1989) found 50 percent less N in non-crusted soils compared

to adjacent crusted soils. Evans and Belnap (1999) found a

42 percent decrease in soil N and a 34 percent decrease in

plant tissue N when comparing a cyanobacterial-moss dominated crust (previously grazed) to an adjacent lichen-dominated (ungrazed) area. In the same area, stable N isotopes

showed that both soil and plants in the lichen-dominated

area contained less newly fixed N than the cyanobacteriamoss dominated area. This has large implications for ecosystems that are dependent on soil crusts for N inputs, such as

found on the Colorado Plateau (Evans and Ehleringer 1993).

As noted above, disturbance also results in increased soil

loss (and thus reduced fertility) via wind and water erosion,

as compressional disturbance breaks apart soil aggregates

formed by the polysaccharide connections. Recent studies

have shown that disturbance of crusted soils increases

sediment loss by up to 300 percent (Belnap and Gillette

1997, 1998; Belnap, unpublished data). After disturbance

and once a soil is stabilized by cyanobacteria, less erosion is

expected compared to the bare soils; however, cyanobacteria

are less able to protect soils from erosion than lichens or

mosses, and thus accelerated losses are expected until the

moss and lichen components recolonize the site. In addition,

burial of nearby biological soil crusts from wind-blown

sediments generally means death for the photosynthetic

components of the soil crusts, further reducing fertility and

stability of these soils. Most of the soil photosynthetic productivity and nitrogen fixation in desert soils is concentrated within 3 mm of the surface (Garcia-Pichel and Belnap

1996).

Conclusion_____________________

Accelerated soil loss is of great concern to land managers

worldwide. Based on this study, soil fertility on the Colorado

Plateau is dependent on the retention of atmospherically

deposited dust and N inputs from lichen-dominated biological soil crusts. Well-developed biological soil crusts reduce

erosional losses. In addition, the crusts contribute substantial amounts of C and N. Current dust deposition rates in the

Colorado Plateau region are low, and when soils are disturbed, loss rates may exceed deposition (Gillette and others

1980; Offer and others 1992; Belnap and Gillette 1997, 1998;

Reynolds and others 1998). Biological soil crusts are easily

disturbed by soil surface disturbances, and recovery is very

slow in this region (Belnap 1993). Thus, it is recommended

that soil surface disturbance be kept to a minimum to

maintain long-term soil fertility and productivity.

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Warren, S.D. 2001a. Biological soil crusts and hydrology in North

American deserts. In: Belnap, J. and O.L. Lange, eds. Biological

soil crusts: structure, function, and management. Ecological

Series 150. Berlin: Springer-Verlag. In press.

Warren, S.D. 2001b. Synopsis: influence of biological soil crusts on

arid land hydrology and soil stability. In: Belnap, J. and O.L.

Lange, eds. Biological soil crusts: structure, function, and management. Ecological Series 150. Berlin: Springer-Verlag. In press.

Williams, J.D.; Dobrowolski, J.P.; West, N.E.; Gillette, D.A. 1995a.

Microphytic crust influence on wind erosion. Transactions of the

American Society of Agricultural Engineers. 38(1):131–137.

Williams, J.D.; Dobrowolski, J.P.; West, N.E. 1995b. Microphytic

crust influence on interrill erosion and infiltration capacity.

Transactions of the American Society of Agricultural Engineers.

38(1):139–146.

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dinitrogen fixation for arid soil rehabilitation. Arid Soil Research

and Rehabilitation. 3:259–265.
154 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Mark Miller is an Ecologist, Bureau of Land Management, Grand Staircase-Escalante National Monument, Kanab, UT 84741. Jayne Belnap is a

Research Ecologist, U.S. Geological Survey, Biological Resources Division,

Moab, UT 84532. Susan Beatty is a Professor of Geography, University of

Colorado, Boulder, CO 80309. Bruce Webb is Soil Scientist, Agronomy and

Horticulture Department, Brigham Young University, Provo, UT 84602.

Components of Spatial and Temporal Soil

Variation at Canyonlands National Park:

Implications for P Dynamics and Cheatgrass

(Bromus tectorum) Performance

Mark Miller

Jayne Belnap

Susan Beatty

Bruce Webb

Abstract—From January 1997 through October 1998, research

was conducted at Canyonlands National Park to investigate soil

traits responsible for distinct spatial patterns of cheatgrass (Bromus

tectorum) occurrence. Field experiments were conducted at sites

representing a broad range of soil conditions and cheatgrass abundances. Standard physicochemical soil measures in combination

with innovative ion-exchange resin capsules and bags were used to

describe spatial and seasonal soil variations. Cheatgrass performance varied along a complex, multivariate soil gradient, with the

strongest cheatgrass-soil relationship occurring during winter. Biogeochemical principles, soil measures, growth rates, and leaf-tissue

analyses support the hypothesis that this complex soil gradient

represents a gradient in P dynamics for cheatgrass. A seasonal

increase in the solubility of carbonate and calcium-phosphate (CaP) compounds should theoretically occur in winter, when cold-moist

soil conditions favor the reaction of CO2 and soil H2O to generate

carbonic acid, H2CO3. The magnitude of this seasonal acidification

phenomenon should vary spatially in relation to pH buffer capacity

(acid-neutralizing potential)—an important component of soil variation that affects Ca-P dynamics. Insights concerning the significance of pH buffer capacity for P dynamics and cheatgrass nutrition

have several implications for research and management.

Introduction ____________________

Distinct soil-vegetation patterns are particularly evident

in arid and semiarid landscapes. In low-precipitation environments, the scarcity of water results in slow rates of

weathering, leaching, and soil formation (Cooke and others

1993). As a consequence, the relative importance of parent

material as a factor determining physicochemical soil properties generally increases with aridity (Birkeland 1999), and

many arid-land vegetation patterns are attributable to

parent-material contrasts (Whittaker and Niering 1968). In

addition, geomorphic processes such as erosion and deposition can produce mosaic landscapes composed of soil patches

differentiated on the basis of pedogenic age and degree of

profile development. Resultant among-soil variations in

profile characteristics can strongly influence vegetation

patterns through effects of pedogenic horizons on spatiotemporal soil-resource dynamics (McAuliffe 1994). Distinct vegetation patterns also may result from topographic variations

(for example, aspect, slope gradient, and slope position) that

affect microclimate, pedogenic processes, and the redistribution of water and mineral elements among landscape

units positioned along a soil catena (Birkeland and Gerson

1991).

Although vegetation patterns often are correlated with

parent materials, profile development, and topography, identification of the ultimate mechanisms underlying these

plant-soil relationships is more problematic and illusive.

Soil variation is complex and multivariate in time and threedimensional physical space, but most plant-soil studies

focus on a very limited set of soil measures (see Hammer

1998 for critique). Because of the significance of water in arid

environments, soil effects on plant water relations often are

emphasized (Comstock and Ehleringer 1992). Nutritional

aspects of plant-soil patterns in arid environments have

received comparatively little attention, despite increasing

evidence for the importance of nutrient relations on population and community dynamics in arid systems (Bilbrough

and Caldwell 1997). Water and nutrient uptake by plants

are not independent (Barber 1995), and Chapin (1991) has

argued that the effects of low soil moisture on nutrient

availability to plants may be almost as significant as the

direct effects of water stress on plant performance. Additional complexity can arise from strong seasonal variations

in soil conditions, such that the availability of limiting soil

resources may vary asynchronously with other limiting

resources or conditions as well as with plant phenology and

resource demand (Bilbrough and Caldwell 1997). Complex,

multi-factor variations in space and time render the elucidation of mechanistic plant-soil relationships a major challenge for ecologists.

A mechanistic understanding of plant-soil patterns is

particularly important with respect to the applied problem

of invasive exotic species. The prediction of potential invasion patterns as well as the ecological restoration of

ecosystems degraded by invasive exotics both depend for
USDA Forest Service Proceedings RMRS-P-21. 2001 155

Components of Spatial and Temporal Soil Variation at Canyonlands National Park... Miller, Belnap, Beatty, and Webb

their success on a solid understanding of the mechanisms

underlying observed invader-environment relationships

(Crawley 1987). In this paper, we examine the plant-soil

mechanisms responsible for distinct spatial patterns in the

distribution and abundance of the invasive exotic grass

cheatgrass (Bromus tectorum L.) in arid landscapes of

Canyonlands National Park, Utah. This research was designed to address two questions. First, what are the major

components of soil variation in the study area? Second, how

does cheatgrass performance vary in relation to identified

components of soil variation? We approached these questions through extensive soil characterization and by conducting field experiments to assess the effects of altered soilresource conditions on seasonal aspects of cheatgrass

performance along a calcareous soil gradient.

Methods _______________________

Study Species

Cheatgrass is an autogamous winter annual grass native

to Eurasia (Mack 1981). Following its introduction to North

America in the late nineteenth century, cheatgrass spread to

most of North America north of Mexico, with the exception of

the southeastern region of the United States (Stubbendieck

and others 1992). It is most abundant in the Intermountain

West, where it reached its present distribution within 50

years of introduction; currently it is the most common

species on >410,000 km2

 of the region (Mack 1981). Cheatgrass seeds typically germinate in response to autumn

precipitation, but recruitment can occur at any time from

autumn through late spring (Mack and Pyke 1983). Germination has been recorded at temperatures just above freezing

(Evans and Young 1972). Seedlings have high rates of root

elongation, and root growth occurs at soil temperatures as

low as 2 to 3 °C (Harris 1967). Comparatively rapid winter

root growth has been cited as a major factor responsible for

cheatgrass’ competitive advantage over native grass seedlings (Harris 1967).

Study Sites

In September 1997, 17 study sites measuring approximately 40 m x 40 m were selected at Canyonlands National

Park (fig. 1). Sites were selected to represent a range in

abundances of cheatgrass and the native C3 bunchgrass

Indian ricegrass (Stipa hymenoides R. & S). Grassland

communities dominated the vegetation at all sites. In addition to cheatgrass and Indian ricegrass, other common taxa

were galleta (Hilaria jamesii [Torr.] Benth.) and dropseeds

(Sporobolus R. Br. spp.). All sites were located at approximately 1550 m in elevation, aspects varied, and slopes

ranged from 0 to 8 percent (Miller 2000). Soils were classified

as mesic Ustollic Camborthids (Begay series) and mesic

Typic Torripsamments (Sheppard series) (USDA Soil Conservation Service 1991).

At each of the 17 sites, six circular ricegrass-centered plots

measuring 1.2 m in diameter were established (102 plots

total). Plots were centered on ricegrass clones to control for

micro-scale soil conditions among the four sets of companion

studies. All litter and plants including the center ricegrass

were removed by hand, and plot interiors (0.8 m diameter)

were seeded with 1150 cheatgrass seeds (~2300 seeds/m2

)

collected at Canyonlands. Seeds were mixed by hand in the

top 1 to 2 cm of soil, and plots were caged with fencing to

exclude vertebrate herbivores and granivores.

Moab

el. 1220 m

Monticello

el. 2149 m

Green R.

Colora do R.

110∞00' 109∞30'

110∞00' 109∞30'

38∞30' 38∞30'

38∞00' 38∞00'

0 5 10 15 20 25 km

Canyonlands

National Park

location of

study sites

Colorado Plateau

Figure 1—Map showing location of study sites in Canyonlands

National Park, Utah.
156 USDA Forest Service Proceedings RMRS-P-21. 2001

Miller, Belnap, Beatty, and Webb Components of Spatial and Temporal Soil Variation at Canyonlands National Park...

Soil Measures

At each site, 10 soil samples were collected systematically

with an 8-cm-diameter bucket auger from each of three

depths 0 to 10, 20 to 30, and 50 to 60 cm. Samples were

composited by depth, air dried, and analyzed by the Plant

and Soil Analysis Laboratory at Brigham Young University

(BYU) for electrical conductivity (EC), pH, cation exchange

capacity (CEC), organic matter content, NaHCO3-extractable P, NH4OAc-extractable K+ (“K-EX”), and acid-neutralizing potential (ANP) following the acid-neutralizing method

of carbonate analysis described by Allison and Moodie (1965).

Measurement of ANP involves reaction of a sample with

dilute HCl, followed by titration to pH 7.0 with NaOH to

determine the quantity of neutralized acid. In soils where

the only acid-neutralizing compounds are carbonates and

bicarbonates (for example, CaCO3 and Ca(HCO3)2), ANP

estimates soil carbonate levels. However, to the degree that

soil constituents other than carbonates (for example, oxides,

hydroxides, and CaSO4) also react with the HCl, this measure is best viewed as a general index of the sample’s total

acid-neutralizing potential (Allison and Moodie 1965). ANP

is the most reactive component of the soil’s total acidneutralizing capacity (ANC) as discussed by van Breemen

(1983), and is conceptually analogous to pH buffer capacity

(Nye 1986).

All macronutrients K+

, HPO4

2–, NH4+

, NO3

–

, Ca2+, Mg2+,

SO4

2–, and micronutrients Mn2+, Zn2+, Fe2+, Cu2+, and Na+

were extracted simultaneously with mixed-bed (cation +

anion) ion-exchange resin “capsules” (acquired from

UNIBEST, Inc., P.O. Box 5095, Bozeman, MT 59717, http:/

/www.wecsa.com/) at BYU following methods described by

Miller (2000). Each manufactured resin capsule consisted of

a 2-cm-diameter spherical ball with 4 ml of mixed-bed resin

beads (H+ - OH– saturated) contained within a plastic screen

mesh. Ion-exchange resin beads and membranes have been

used for laboratory and in-situ nutrient measurements for

over 40 years (see Skogley and Dobermann 1996 for review).

The approach used here, with a simultaneous resin extraction of multiple elements from a saturated paste, has been

referred to as the “phytoavailability soil test” (PST) (Skogley

and Dobermann 1996). The PST provides an integrated

index of nutrient bioavailability because it is sensitive to ion

activities in the soil solution, as well as to ion diffusion and

other soil properties that are important components of soil

nutrient buffering capacity (Skogley and others 1990).

Soils were analyzed by the U.S. Geological Survey (USGS)

Central Region Geology Laboratory, Denver, for particle

size, carbonate content, and magnetic susceptibility. Particle size was measured with a Malvern laser particle sizer

following the removal of carbonates and organic material by

acid digestion. Carbonate content was determined gasometrically by measuring the volume of evolved CO2 produced by reacting a sample with acid (Dreimanis 1962).

Magnetic susceptibility (MS) measurements were conducted

with a susceptometer. MS is a rapid, non-destructive measure

that provides an index of the concentration of magnetic

grains in a sample (Mullins 1977). Among-soil variations in

MS have been interpreted to result from pedogenic processes

(Singer and Fine 1989) or aeolian deposition of silt-sized

particles bearing magnetic minerals (Reynolds and King

1995; Hanson 1999).

To assess in-situ nutrient dynamics, at five sites four

nylon-mesh bags containing 10 g of moist, mixed-bed ionexchange resins (H+ - Cl– saturated) were buried in all

experimental plots at depths of 5 to 10 cm (Lajtha 1988). Ionexchange resin bags were first placed at the beginning of

experimentation in January 1997 and were replaced seasonally thereafter (approximately 3-month intervals). After

replacement, exposed resin bags were extracted with HCl

and analyzed for macro- and micronutrients at BYU.

Cheatgrass Measures

Cheatgrass measurements were made once following germination in October, at the onset of winter in early December, and monthly in spring from mid-March to mid-May. Fall

establishment was estimated in December by counting the

number of live plants occurring in a rectangular 250-cm2

quadrat frame aligned with each of the four cardinal directions in each plot (1000 cm2 sampled per plot). Ten individual plants per plot (1020 total) were marked with numbered sticks in late October. Total leaf lengths (sheaths plus

blades) of all marked plants were measured to the nearest

mm, averaged to obtain a single measure per plot per growth

period, and used to calculate relative growth rates (mm/mm/

day). In spring, foliar tissues were collected from plants in a

subset of plots. Tissues were air dried, ground, and analyzed

at BYU for tissue concentrations (percent dry weight) of

mineral elements following wet digestion. At the end of the

growing season, above-ground tissues were harvested, air

dried, and weighed to obtain total biomass per plot.

Statistical Analyses

To describe among-site soil variation, 40 soil variables

were analyzed by principal components analysis (PCA) with

varimax factor rotation (Kent and Coker 1992). Included in

the analysis were soil measures from 0 to 10 cm, total profile

values for macro- and micronutrients (sum of resin-capsule

values for 0 to 10, 20 to 30, and 50 to 60 cm samples within

a single core), and the surface:depth ratio for ANP (0 to 10

cm:50 to 60 cm ratio), the latter measure providing an index

of profile development. Simple linear correlation (Zar 1999)

was used to assess relationships between seasonal measures

of cheatgrass performance and spatial components of soil

variation identified through PCA. All statistical analyses

were conducted using the software package STATISTICATM

v5.5 on a PC platform (StatSoft 1999).

Results ________________________

Soil Variation

Table 1 summarizes selected soil characteristics of the 17

study sites considered together as a group. In general, study

area soils were sandy and calcareous. Soil ANP tended to be

slightly higher and more variable than carbonate content,

suggesting the presence of acid-neutralizing compounds in

addition to carbonates. Soils had low organic-matter (OM)

content, low CEC, and low levels of NaHCO3-extractable P.

Resin-capsule data indicated that Ca2+ was the most active

cation in the soil environment, with values 8-9 times higher
USDA Forest Service Proceedings RMRS-P-21. 2001 157

Components of Spatial and Temporal Soil Variation at Canyonlands National Park... Miller, Belnap, Beatty, and Webb

Table 1—Descriptive statistics for selected soil characteristics of 17 study sites at Canyonlands National Park, Utah.

Variable (units) Mean Min. Max. s.d. CVa

0 to 10 cm

Acid-neutralizing potential (% CaCO3 equiv.) 7.35 4.41 11.03 2.08 28.27

Carbonate content (% CaCO3 equiv.) 6.45 5.02 8.20 1.02 15.80

Magnetic susceptibility (m3

/kg x 10–8) 7.26 2.59 14.83 3.94 54.27

Coarse sand (%) 15.26 7.70 24.23 4.48 29.33

Fine sand (%) 70.74 61.93 77.60 4.06 5.74

Total sand (%) 86.01 77.30 90.38 3.86 4.49

Silt (%) 9.97 6.03 17.00 3.07 30.80

Clay (%) 4.02 2.83 5.74 0.89 22.10

pH 7.50 7.17 7.99 0.22 2.96

EC (dS/m) 0.38 0.28 0.46 0.05 13.10

CEC (cmolc/kg soil) 4.52 1.74 8.74 1.82 40.21

Organic matter (%) 0.26 0.04 0.42 0.10 40.73

K-EX (ppm) 168.46 86.92 323.60 61.49 36.50

NaHCO3-P (ppm) 7.98 4.02 14.34 2.43 30.45

K (μmolc/capsule) 39.64 23.42 61.80 10.15 25.60

HPO4 (μmolc/capsule) 10.87 4.91 18.02 4.46 41.01

NH4 (μmolc/capsule) 14.40 6.51 21.49 5.22 36.25

NO3 (μmolc/capsule) 2.79 0.33 6.18 1.82 65.23

Ca (μmolc/capsule) 990.55 491.03 1973.42 423.64 42.77

Mg (μmolc/capsule) 111.48 40.92 252.39 63.54 57.00

SO4 (μmolc/capsule) 27.66 15.98 48.88 10.14 36.65

Mn (μmolc/capsule) 2.00 0.84 3.63 0.95 47.75

Zn (μmolc/capsule) 0.25 0.10 0.64 0.15 59.26

Fe (μmolc/capsule) 4.90 3.41 6.73 1.06 21.61

Cu (μmolc/capsule) 0.12 0.06 0.20 0.04 35.27

Na (μmolc/capsule) 9.25 1.79 16.08 5.30 57.36

Surface:depth (0 to 10 : 50 to 60 cm)

Acid-neutralizing potential 0.76 0.32 1.07 0.21 27.59

K 1.20 0.47 2.50 0.61 50.67

HPO4 2.73 1.21 8.14 1.55 57.00

NH4 1.33 0.54 3.00 0.68 50.89

NO3 1.72 0.14 10.01 2.33 135.47

Ca 0.94 0.41 2.28 0.40 42.52

Mg 1.05 0.54 2.31 0.38 36.37

SO4 0.89 0.18 2.08 0.37 41.77

Mn 2.28 0.86 5.28 1.13 49.66

Zn 1.37 0.45 3.05 0.64 47.16

Fe 1.08 0.75 1.37 0.18 17.04

Cu 1.19 0.70 1.91 0.31 25.97

Na 1.20 0.02 7.21 1.62 134.94

HPO4:Ca 3.06 1.52 6.99 1.50 49.07

Mn:Ca 2.69 1.01 7.23 1.68 62.31

a

CV = coefficient of variation (100*s.d./mean).

(on a charge basis) than Mg2+, the second most active cation.

Together, these two accounted for approximately 94 percent

of measured cation charges. Of the measured anions, SO4

2–

was the most active. Measured anions reported in table 1

provided less than 5 percent of the charges required to

balance measured soil cations. Based on water analysis

(Miller 2000), it is probable that HCO3

– was the major

charge-balancing anion in the soil.

Surface:depth ratios in table 1 indicate several soil-profile

trends. On average, ANP, Ca2+, and SO4

2– tended to increase

with depth whereas K+

, HPO4

2–, N, and micronutrients

tended to have higher values at the surface than at depth.

HPO4

2–:Ca2+ and Mn2+:Ca2+ ratios also tended to be much

higher at the surface than at the 50 to 60 cm depth. NO3

–

levels were extremely variable in the sampled profiles. Of

the single-ion measures, average, minimum, and maximum

surface:depth ratios were greatest for HPO4

2– and Mn2+

(with the exception of the maximum value for NO3

–

), indicating a strong tendency for resin-extractable P and Mn both to

be concentrated at the soil surface.

The first four axes derived from the PCA of soil variables

explained 62 percent of the variation in the analyzed data set

(table 2). Variables with highly significant (p<0.01) positive

loadings for the first axis included 0 to 10 cm carbonate

content, HPO4

2–, Ca2+, Mg2+, SO42–, Mn2+, and Na+

; and

total-profile HPO4

2–, Ca2+, Mg2+, and Mn2+. The second PCA

axis was characterized by high positive loadings for 0 to 10

cm ANP and sand content, as well as for the ANP

surface:depth ratio. Variables with high negative loadings

for axis II included 0 to 10 cm MS, percent silt and clay, CEC,
158 USDA Forest Service Proceedings RMRS-P-21. 2001

Miller, Belnap, Beatty, and Webb Components of Spatial and Temporal Soil Variation at Canyonlands National Park...

Table 2—Summary of the first four axes derived from principal-components analyses (PCA) of soil data describing

17 study sites at Canyonlands National Park, Utah. For surface:depth variables, only significant

correlations are reported.

PCA Axes

I II III IV

Proportion of variation explained 0.23 0.17 0.13 0.09

Variable correlations (loadings for included variables)

0 to 10 cm

Acid-neutralizing potential 0.18 0.78*** –0.22 –0.14

Carbonate content 0.86*** 0.22 0.15 0.11

Magnetic susceptibility –0.24 –0.91*** 0.07 –0.07

Coarse sand 0.17 0.48 –0.10 –0.08

Fine sand 0.02 0.25 0.06 0.37

Total sand 0.21 0.82*** –0.05 0.30

Silt –0.13 –0.82*** 0.09 –0.28

Clay –0.44 –0.71*** –0.08 –0.31

pH –0.16 –0.12 0.17 0.81***

EC –0.25 –0.30 –0.06 –0.21

CEC –0.34 –0.74*** –0.13 –0.17

Organic matter 0.09 –0.56* 0.50* 0.11

K-EX –0.10 –0.88*** –0.12 0.11

K 0.39 –0.35 0.33 0.66**

HPO4 0.63** –0.14 0.45 0.05

HPO4:Ca1 –0.33 –0.78*** 0.12 0.06

NH4 0.22 –0.04 0.91*** 0.19

NO3 –0.40 0.20 0.40 –0.03

NH4+NO3 0.07 0.03 0.93*** 0.16

Ca 0.65** 0.18 0.37 0.03

Mg 0.91*** 0.27 –0.01 0.15

SO4 0.70** 0.17 0.35 0.05

Mn 0.85*** 0.17 0.14 0.03

Mn:Ca1 0.58* –0.01 –0.19 0.01

Zn 0.40 0.19 0.12 0.81***

Fe 0.30 0.21 0.14 0.02

Cu 0.44 0.13 0.48 0.15

Na 0.75*** 0.02 0.46 –0.07

Total profile sum (sum 0 to 10, 20 to 30, and 50 to 60 cm)

K 0.37 0.19 0.25 0.68**

HPO4 0.71*** 0.06 0.33 0.13

NH4 0.44 –0.07 0.66 0.14

NO3 –0.07 0.01 0.58 0.06

NH4+NO3 0.33 –0.06 0.70*** 0.13

Ca 0.70** 0.16 0.23 0.18

Mg 0.86*** 0.30 –0.05 0.20

SO4 0.42 0.10 0.28 0.05

Mn 0.88*** 0.32 0.06 0.07

Zn 0.08 0.32 0.06 0.79***

Fe 0.46 0.26 0.33 0.14

Cu 0.36 0.15 0.44 0.27

Na 0.14 0.04 0.25 –0.05

Surface:depth ratio (0 to 10 : 50 to 60 cm ratio)

Acid-neutralizing potential 0.31 0.76*** 0.25 –0.17

K1 –0.38 –0.68** 0.03 0.13

HPO4:Ca1 –0.33 –0.80*** –0.23 0.07

NH4

1 –0.26 0.09 0.52* 0.27

Ca1 0.03 0.13 0.53* –0.26

Mn1 –0.36 –0.51* 0.10 –0.06

Mn:Ca1 –0.40 –0.69** –0.33 0.14

Zn1 0.37 0.08 0.30 0.74***

1

Not included in PCA; * p <0.05; ** p <0.01; *** p <0.001
USDA Forest Service Proceedings RMRS-P-21. 2001 159

Components of Spatial and Temporal Soil Variation at Canyonlands National Park... Miller, Belnap, Beatty, and Webb

K-Ex. Other soil measures that were significantly inversely

correlated with axis II (though not included in the PCA) were

the 0 to 10 cm HPO4

2–:Ca2+ ratio, as well as surface:depth

ratios for K+

, HPO4

2–:Ca2+, and Mn:Ca2+. Correlations of

surface:depth HPO4

2–with PCA axes were highly influenced

by a single outlier. Removal of the outlier also resulted in a

significant inverse correlation of surface:depth HPO4

2– with

axis II (r = –0.71, p <0.05). Variables with highly significant

loadings for axis III were 0- to –10-cm and total-profile NH4

+

and NH4

+

+NO3

–

. The fourth axis was characterized by high

loadings for 0- to –10-cm pH, K+

, and Zn2+, as well as totalprofile K+ and Zn2+. The surface:depth ratio for Zn2+ also was

correlated with axis III, although not included in the PCA.

Cheatgrass performance measures were most highly and

consistently correlated with axis II (table 3). Performance

also was correlated with axis IV, though to a lesser degree.

A plot of significant soil variables in relation to these two

PCA axes shows that axis II can be conceptualized as a

complex soil gradient (fig. 2). At one end of the conceptual

soil gradient (high axis-II scores) were sandy sites characterized by high ANP and high surface:depth ANP. Maximum

surface:depth ANP in the data set was 1.07 (table 1), indicating a lack of profile differentiation at that end of the gradient. At the other end of the conceptual gradient (low axis-II

scores) were sites with higher silt and clay content, as well

as greater CEC, K-EX, OM, and HPO4

2–:Ca2+ values at 0 to

10 cm. At this extreme of the gradient, low surface:depth

ANP was associated with high surface:depth HPO4

2–:Ca2+,

K+

, Mn2+, and Mn2+:Ca2+. These measures, all indicative of

profile differentiation, tended to covary with MS in 0 to 10

cm soils. Variations in profile differentiation along the

conceptual gradient were consistent with taxonomic identity. Soils with differentiated profiles generally were classified as Camborthids, whereas soils without profile differentiation generally were classified as Torripsamments (USDA

Soil Conservation Service 1991).

Cheatgrass Performance

Figure 3 summarizes seasonal variations in cheatgrass

performance in relation to selected soil variables and PCA

axes II and IV. Net cheatgrass establishment in fall was

greatest at relatively fine-textured sites with low ANP and

high HPO4

2–:Ca2+ values. Among-soil patterns in fall growth

rates tended to parallel establishment patterns. Winter

(early December to mid-March) growth rates varied linearly

along the conceptual soil gradient described by PCA axis II

(Pearson’s r = –0.78, p <0.001, table 3). It was during this

3-month winter period that the greatest relationship of

cheatgrass performance to measured soil variation was

found, with the highest growth rates found in low-ANP, finetextured soils. Relative growth rates increased markedly in

early spring, but sites with the highest winter growth rates

consistently had the lowest growth rates during both the

early and mid-spring periods (Miller 2000). Spring growth

was greatest at sites that were intermediately positioned

along PCA axis II and high on PCA axis IV (fig. 3). By the end

of the growing season, whole-plot biomass tended to be

greater at these intermediate sites, but the biomass difference between sites where cheatgrass performed best during

fall and winter and sites where cheatgrass performed best

during spring was statistically insignificant (Miller 2000).

Data from resin bags in plots at selected study sites

provide information concerning in-situ nutrient dynamics

during the fall-winter-spring cheatgrass growing season.

During the January to April winter period when cheatgrass

performance varied inversely with soil ANP and PCA axis II,

resin-bag Mn2+, HPO4

2–, K+

, and Mg2+ also varied inversely

with soil ANP (fig. 4). Ca2+ and Fe varied positively with

ANP during this period, and correlations of NH4

+ and NO3–

with ANP were insignificant (fig. 4).

In figure 5, leaf-tissue nutrient concentrations for cheatgrass in this study are compared with concentrations reported for cheatgrass in shrubsteppe environments of southcentral Washington (Rickard and Vaughan 1988), values for

the native winter-annual grass sixweeks fescue (Festuca

octoflora Walter) in sandy, calcareous soils of southeastern

Utah (Belnap and Harper 1995), and average mineral contents reported to be adequate for unrestrained plant growth

(Epstein 1965, cited in Marschner 1995). Average tissue N

(2.02 percent) and K (1.28 percent) for cheatgrass in this

study were higher than or similar to values reported for

cheatgrass in Washington, sixweeks fescue in Utah, and

average values for unrestrained plant growth. In contrast,

concentrations of the carbonate-related minerals P (0.08

percent), Ca (0.35 percent), Mg (0.09 percent), and Mn (0.004

percent) all were lower in this study than in the comparative

data sets. Of these, P content was the lowest in comparison

with concentrations reported elsewhere. Tissue Fe (0.04

percent), N:P, and K:P documented in this study all tended

to be much higher than comparative values.

Table 3—Correlation coefficients (Pearson’s r) describing relationships among cheatgrass performance measures

and axes I to IV derived from principal components analyses of soil characteristics, Canyonlands

National Park, Utah. Performance measures used in the analyses were site averages with all

manipulative treatments combined (n = 17). (RGR = relative growth rate.)

PCA Axes

Performance measure I II III IV

Net fall establishment –0.38 –0.51* 0.31 0.02

RGR, Oct. to Dec. 0.15 –0.53* –0.12 –0.07

RGR, Dec. to Mar. –0.40 –0.78*** 0.14 0.17

RGR, Mar. to Apr. 0.38 0.10 0.03 0.55*

RGR, Apr. to May 0.44 0.49* 0.11 0.34

End-of-season biomass 0.06 –0.35 0.10 0.44

* p <0.05; ** p <0.01; *** p <0.001
160 USDA Forest Service Proceedings RMRS-P-21. 2001

Miller, Belnap, Beatty, and Webb Components of Spatial and Temporal Soil Variation at Canyonlands National Park...

Discussion _____________________

Results presented here demonstrate the complex, multivariate nature of soil variation and plant-soil relationships.

Cheatgrass-soil relationships varied by season and performance measure, but the most significant pattern occurred

during the 3-month December to March period when

cheatgrass growth varied strongly in relation to PCA axis II.

Winter growth varied positively with 0 to 10 cm silt and clay

content, CEC, K-Ex, MS, and resin-capsule HPO4

2–:Ca2+,

whereas growth varied inversely with both 0 to 10 cm and

surface:depth ANP. Which of these variables, either alone or

in combination, best explains winter variations in cheatgrass

growth along the conceptual soil gradient described by PCA

axis II?

CEC is considered an important component of soil fertility

(Brady and Weil 1996). In this study, CEC and K-EX both

covaried with silt and clay content, consistent with the

pattern observed for most soils (Brady and Weil 1996).

However, with the important exceptions of NH4

+ and K+

, the

availabilities of most nutrient cations (Ca2+, Mg2+, Mn2+,

Cu2+, Zn2+, Fe2+) to plants in calcareous soils are likely to be

more strongly influenced by carbonate reactions (including

sorption, desorption, precipitation, dissolution, and pH buffering) than by ion-exchange properties of soil colloids (Knight

1991). On the basis of resin-capsule data, it can be inferred

that Ca2+ and Mg2+ together occupied approximately 94

percent of the exchange sites on soil colloids. Resin bags

buried at five study sites indicated that in-situ NH4

+

Correlation with Axis IV (Pearson's r)

-0.6

-0.4

-0.2

0.0

0.2

0.4

0.6

0.8

1.0

0-10 cm

Total profile,

0-10, 20-30, 50-60 cm

combined

Surface:depth ratio,

0-10:50-60 cm

K

MS

silt clay

CEC

Mn

K-Ex OM

K

pH

Zn

Zn Zn

K

sand

ANP

ANP

P:Ca

Mn:Ca

Correlation with Axis II (Pearson's r)

-1.0 -0.8 -0.6 -0.4 -0.2 0.0 0.2 0.4 0.6 0.8 1.0

Figure 2—Plot of soil variables significantly correlated

with PCA axes II and IV, Canyonlands National Park.

Correlation with Axis IV (Pearson's r)

-0.6

-0.4

-0.2

0.0

0.2

0.4

0.6

0.8

1.0

silt clay

K

pH Zn

sand

ANP

P:Ca

Correlation with Axis II (Pearson's r)

-1.0 -0.8 -0.6 -0.4 -0.2 0.0 0.2 0.4 0.6 0.8 1.0

Fall Establ

Fall RGR

Winter RGR

E Spr RGR

Mid-Spr RGR

End Biom

Figure 3—Vector plot illustrating correlations of seasonal cheatgrass measures with soil PCA axes II and

IV, Canyonlands National Park.

-1.0

-0.8

-0.6

-0.4

-0.2

0.0

0.2

0.4

0.6

0.8

1.0

Mn P K Mg Ca Fe NH4 NO3

Correlation with ANP

(Pearson's r)

*** ***

***

 

** 

Jan. to Apr. Resin-bag Measure

*** p < 0.001

 ** p < 0.01

Figure 4—Correlations of in-situ resin-bag measures

with soil acid-neutralizing potential, January to April

1998, Canyonlands National Park.

Figure 5—Comparison of average mineral contents of

cheatgrass at Canyonlands National Park (this study)

with those of cheatgrass in shrubsteppe environments

of south-central Washington (Rickard and Vaughan

1988) and those of the native annual grass sixweeks

fescue (Festuca octoflora) in southeastern Utah near

Canyonlands (Belnap and Harper 1995). Values on

the y-axis were derived by dividing observed mineral

contents by average mineral contents reported to be

adequate for unrestrained plant growth (Epstein 1965,

cited in Marschner 1995). For cheatgrass in this study,

error bars extend 1 SE above means (n = 30). Observed:adequate ratio

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

4.0

4.5

N K P Ca Mg Mn Fe N:P K:P

Cheatgrass, this study

Cheatgrass, WA

Sixweeks fescue, UT

n.d. n.d. n.d.
USDA Forest Service Proceedings RMRS-P-21. 2001 161

Components of Spatial and Temporal Soil Variation at Canyonlands National Park... Miller, Belnap, Beatty, and Webb

adsorption did not vary in relation to CEC or axis II during

winter. In-situ K+ was weakly correlated with CEC and axis

II during the winter period, but KCl additions did not

enhance cheatgrass performance during any period (Miller

2000). These observations suggest that variations in CEC

and K-Ex cannot alone explain winter variations in cheatgrass

performance along axis II. MS, because it simply serves as a

proxy indicator of variations in aeolian silt content (Reynolds

and King 1995; Hanson 1999) and/or pedogenic profile

development (Singer and Fine 1989), by itself cannot provide a mechanistic explanation for spatial variations in

cheatgrass performance.

In contrast with CEC, K-Ex, and MS, ANP can provide a

mechanistic explanation for winter variations in cheatgrass

performance due to the importance of rhizosphere acids for

plant nutrition in calcareous soils. Chemical conditions in

the rhizosphere are known to be drastically different than

bulk-soil measures as a consequence of biotic processes

(Hinsinger 1998). In calcareous soils, solubilities of nutrients P, Mn, Zn, and Fe typically are low due to one or more

of the following interrelated geochemical factors: (1) sorption reactions with carbonate minerals, (2) the formation of

insoluble Ca and/or carbonate compounds, and (3) the presence of high Ca2+ and HCO3

– levels which further inhibit

nutrient dissolution due to common-ion effects and/or acidneutralization reactions (Barber 1995). Rhizosphere acidification due to the combined activities of roots, mycorrhizal

symbionts, and associated rhizosphere microbes is a common means by which nutrient dissolution and acquisition

can be enhanced in calcareous soils (Hinsinger 1998). Rhizosphere acidification most often is caused by protons excreted

to balance uptake of cations such as NH4

+ and Ca2+ (Haynes

1990), but respiratory CO2 also can be an important acidification mechanism through its reaction with H2O to form

carbonic acid, H2CO3 (Hinsinger 1998).

The generation of H2CO3 in the soil environment depends

on (1) the partial pressure of CO2, (2) soil water content, and

(3) CO2 solubility in H2O (Krauskopf and Bird 1995). CO2

solubility in H2O, like that of other gases, is greater at cold

temperatures than at warm temperatures (Krauskopf and

Bird 1995). Thus, all else being equal, H2CO3 formation in

the soil environment should exhibit a seasonal increase

during winter when soils are moist and cold. Cheatgrass also

exhibits considerable below-ground growth during winter

(Harris 1967), presumably producing respiratory CO2, enhancing rhizosphere H2CO3 generation, and facilitating the

dissolution and acquisition of carbonate-bound nutrients.

The enhancement of nutrient dissolution and acquisition

due to rhizosphere H2CO3 generation is a temporal phenomenon, and the magnitude of this temporal phenomenon

should vary spatially in relation to soil characteristics. The

major soil properties influencing soil susceptibility to plantinduced rhizosphere acidification are initial soil pH and soil

pH buffer capacity (Marschner and Römheld 1996), the

latter measured here as ANP. Rhizosphere pH, which cannot be measured from bulk soil samples, is strongly dependent on pH buffer capacity (Marschner and Römheld 1996).

Accordingly, ANP or other indices of pH buffer capacity

should be more widely applied in studies of plant-soil relationships because they describe a dynamic, plant-relevant

soil property that cannot be inferred from static pH

measurements alone. Measured pH can vary due to differences in soil texture (as it effects soil water capacity), salt

concentrations, and technique; pH buffer capacity can vary

widely among soils in which pH varies only slightly (van

Breemen and others 1983; Bache 1984).

Data from in-situ resin bags and leaf tissues suggest that

the conceptual soil gradient associated with ANP and PCA

axis II was a gradient in P and Mn bioavailability for

cheatgrass. Resin-bag HPO4

2– and Mn2+ covaried in relation

to PCA axis II and ANP similar to the among-site pattern

observed for winter cheatgrass growth. Although average

tissue P and Mn concentrations for cheatgrass in this study

both were lower than “adequate” levels reported by Epstein

(1965, cited in Marschner 1995), Mn concentrations were 3

to 4 times greater than those “critical” for growth of agronomic monocots (Hannam and Ohki 1988). DeLucia and

others (1989) found experimentally that cheatgrass was Plimited in hydrothermally altered soils possessing NaHCO3-

extractable-P levels similar to those found in Canyonlands

soils. Thus the evidence suggests that PCA axis II, in

association with ANP, primarily was a gradient in P limitation for cheatgrass.

Conclusions____________________

Findings of this study emphasize the complex nature of

plant-soil interactions and the importance of temporal plantsoil dynamics for understanding spatial plant-soil patterns.

Cheatgrass performance varied along a complex, conceptual

soil gradient characterized by variations in particle size,

acid-neutralizing potential (pH buffer capacity), exchangeable K, and several profile indices indicative both of pedogenesis and of plant-soil feedbacks. Cheatgrass-soil relationships

were strongest during winter when relative growth rates

were inversely correlated with acid-neutralizing potential

and positively correlated with silt and clay content and

exchangeable K. Biogeochemical principles, as well as evidence from in-situ resin bags, tissue chemistry, and experimental manipulations of K availability suggest that this

conceptual soil gradient primarily was a gradient of P

limitation for Bromus. We hypothesize that spatial variations in soil acid-neutralizing potential affected the degree

to which P dissolution and acquisition were enhanced in

winter by the formation of carbonic acid in cold, moist soils.

The complex space-time dynamics described here indicate

the need for ecological plant-soil studies to expand and

investigate a broader range of resources and relationships.

Acknowledgments ______________

Major funding for this work was provided through a STAR

Graduate Education Fellowship awarded to MM by the U.S.

Environmental Protection Agency and by research funding

awarded to JB by the U.S. Geological Survey. Additional

financial support was provided by the Dean of the Graduate

College at the University of Colorado-Boulder and the Biogeography Specialty Group of the Association of American

Geographers. Ann Welshko and Lean Henri assisted both in

the field and in the lab. Cooperation and support of

Canyonlands National Park made this work possible.
162 USDA Forest Service Proceedings RMRS-P-21. 2001

Miller, Belnap, Beatty, and Webb Components of Spatial and Temporal Soil Variation at Canyonlands National Park...

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USDA Forest Service Proceedings RMRS-P-21. 2001 163

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

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Angela D. Yu is a Graduate Student, Department of Geography, University of Colorado at Boulder, Boulder, CO 80309-0030. Simon A. Lei is a

Biology and Ecology Professor at the Community College of Southern

Nevada, 6375 West Charleston Boulevard, WDB, Las Vegas, NV 89146-

1139.

Abstract—The topography, climatic pattern, location, and origin of

islands generate unique patterns of species distribution. The equilibrium theory of island biogeography creates a general framework

in which the study of taxon distribution and broad island trends

may be conducted. Critical components of the equilibrium theory

include the species-area relationship, island-mainland relationship, dispersal mechanisms, and species turnover. Because of the

theoretical similarities between islands and fragmented mainland

landscapes, reserve conservation efforts have attempted to apply

the theory of island biogeography to improve continental reserve

designs, and to provide insight into metapopulation dynamics and

the SLOSS debate. However, due to extensive negative anthropogenic activities, overexploitation of resources, habitat destruction,

as well as introduction of exotic species and associated foreign

diseases (biological invasions), island conservation has recently

become a pressing issue itself. The objective of this article is to

analyze previously published data, and to review theories from

numerous research studies that attempt to explain species patterns

on islands. In effect, this analysis brings insight into current issues

of continental reserve design and island conservation efforts.

Introduction ____________________

The equilibrium theory of island biogeography (ETIB),

proposed by MacArthur and Wilson, is a relatively recent

development that has sparked a tremendous amount of

scientific controversy. Initially introduced to the public in

1963 as “An Equilibrium Theory of Insular Zoogeography,”

the idea was expanded in 1967 into a book publication. The

ETIB implies that island fauna and flora (biota) eventually

reach an equilibrium point between extinction and immigration. Although species rarely reach equilibrium due to the

extremely dynamic island system, MacArthur and Wilson

note that the ETIB permits general predictions of future

island biodiversity patterns. In this article, the theory of

island biogeography is examined in reference to island

environments, including topographic origins and characteristics, as well as climatic patterns. A comprehensive

analysis of the theory is discussed, such as species-area

Equilibrium Theory of Island

Biogeography: A Review

Angela D. Yu

Simon A. Lei

relationship, dispersal mechanisms and their response to

isolation, and species turnover. Additionally, conservation

of oceanic and continental (habitat) islands is examined in

relation to minimum viable populations and areas,

metapopulation dynamics, and continental reserve design.

Finally, adverse anthropogenic impacts on island ecosystems are investigated, including overexploitation of resources, habitat destruction, and introduction of exotic species and diseases (biological invasions). Throughout this

article, theories of many researchers are re-introduced and

utilized in an analytical manner. The objective of this article

is to review previously published data, and to reveal if any

classical and emergent theories may be brought into the

study of island biogeography and its relevance to mainland

ecosystem patterns.

Island Environments _____________

Island Formation and Topography

Island topography is primarily determined by the geophysical origins of the island. Marine islands may be subdivided into two geophysically distinct categories: continental

shelf islands (land-bridge islands) and oceanic islands. Continental shelf islands are likely to be physically connected to

the mainland during low sea level periods. Due to their

connection, these islands have similar geological structure

to the nearby mainland (Williamson 1981). This similar

topography, coupled with the island’s close proximity to the

continent, results in the proliferation of similar flora and

fauna (biota).

Oceanic islands are typically more isolated, and may have

never been physically connected to a continental landmass.

There are three main types of oceanic islands: oceanic ridge

islands, hot-spot islands, and the individual islands of island

arcs. Oceanic ridge islands and hot-spot islands are volcanic

islands because they are formed from ocean-floor volcanoes.

Islands that are part of island arcs also have a volcanic

origin, involving the collision of continental and oceanic

plates, resulting in islands that consist of both basalt and

granite rock (Williamson 1981).

All of the geological processes occurring volcanic islands

can produce islands with high elevations, with peaks of at

least 2,000 m (fig. 1) (Williamson 1981). Volcanic islands are

typically steeper and become increasingly dissected with

age. This phenomenon has important implications for island

biota because a wide range of elevational gradients and

associated ecological attributes allows for the persistence of

diverse habitats. The elevation of islands also has important influences on the climatic regime.
164 USDA Forest Service Proceedings RMRS-P-21. 2001

Yu and Lei Equilibrium Theory of Island Biogeography: A Review

Island Climate

Island climate is determined by both external influences,

such as ocean circulation and atmospheric circulation, and

internal influences, such as island size, shape, and topography. Ocean circulation and atmospheric circulation consist

of water currents and air currents, respectively, that have

similar movements of upwelling and sinking. If an island is

in the path of a moving current or is located where two

currents intersect, this can alter the climate significantly. In

addition to circulation influences, the proximity of an island

to a continental landmass also affects the island’s climate.

Islands located close to a mainland, such as land-bridge

islands, are likely to be influenced by the continental climate. Remote oceanic islands, on the contrary, are influenced by the maritime climate.

Internal influences, such as island size and elevation, can

have a substantial impact on the precipitation regime on the

island. Whittaker (1998) states that low islands typically

have relatively dry climates and high islands are wetter

through orographic rainfall, resulting in the creation of

extensive arid regions due to the rain shadow effect. These

higher islands often contain diverse habitats within a relatively small area. Due to the impact of elevation on island

climate, research studies have indicated that elevation is a

critical variable in analyzing species diversity on islands.

Telescoping, a compression of elevational zones, is fairly

common on small tropical islands. Leuschner (1996) proposes

that forest lines on islands are generally 1,000 to 2,000 m

lower than forest lines on continents. Hence, telescoping

creates smaller patches from a variety of habitats favorable

to many species, and permits high- and low-elevation inhabiting species to coexist in a relatively small area (Whittaker

1998).

Island Patterns _________________

The Equilibrium Theory of Island Biogeography (ETIB)

revolutionizes the way in which biogeographers and ecologists viewed island ecosystems. Prior to the ETIB was the

static theory of islands (Dexter 1978), which hypothesizes

that island community structures remain relatively constant over geological time. The only mechanism for biological change was the gradual evolutionary process of speciation. Few successful colonization events would occur due to

a limited number of ecological niches on the island (Lack

1976). Once these niches are completely filled, no space and

resources are available for new immigrants, and they may

not become successfully established on the island. The ETIB

refutes the static theory, indicating that island communities

exhibit a dynamic equilibrium between species colonization

and extinction, or species turnover. The immigration curve

is descending and is shaped concavely because the most

successful dispersing species would colonize initially, followed by a significant decrease in the overall rate of immigration (fig. 2). The extinction curve, on the contrary, is an

ascending curve because as more species inhabit the island

through time, more species would become extinct exponentially (fig. 2). Such a trend is amplified due to a combination

of population size and negative biotic interactions among

Figure 1—A map indicating all islands with a peak of 2000 m or higher. Larger islands are

shaded, smaller islands are denoted by ∆ (Williamson 1981).
USDA Forest Service Proceedings RMRS-P-21. 2001 165

Equilibrium Theory of Island Biogeography: A Review Yu and Lei

different species. This model graphically and mathematically represents an equilibrium point, S, in which the immigration and extinction curves intersect (fig. 2). This point

represents the actual number of species present on an island

at equilibrium. Moreover, figure 3 accounts for trends in

island size and degree of island isolation (distance from

mainland). Patterns regarding the species-area relationship and the species-isolation relationship have been acknowledged by biogeographers since the beginning of the

19th century. Therefore, the contribution made to island

ecosystem study by MacArthur and Wilson was a compilation of these well-known ideas into one, integrated paradigm

(Brown and Lomolino 1998).

Species-Area Relationship

A positive relationship exists between island size and

island species richness (fig. 4). These two variables, nevertheless, do not always exhibit a linear correlation. Arrhenius

represented this non-linear trend in mathematical form in

1920 with the following equation:

S = cAZ

In this equation, S = the species richness on an island, c = a

constant depending on biotic and biogeographic region,

A = the area of the island, and z = a constant representing the

slope of S and A on a logarithmic scale (z changes very little

among different taxa or same taxon from different regions.).

There are two potential explanations for the positive

correlation between island size and species diversity. First,

large islands generally contain more diverse habitats and,

thus, more biota compared to small islands. Although this is

a logical explanation, ecologists and biogeographers have a

difficulty to prove in the field because habitat diversity has

no distinct parameters and is a challenge to measure. Many

parameters are approximated to determine the number of

species inhabiting various islands. Second, the island size,

rather than the habitat diversity, is the main factor in

determining the number of species on islands. This theory is

also difficult to prove in the field because habitat diversity

and island size are strongly correlated, and it is nearly

impossible to distinguish the two.

Species-Isolation Relationship

(Distance Effect)

Isolation is a critical component when examining evolutionary processes since it allows for allopatric speciation to

occur. Islands offer prime examples of isolation effects on

biota (Cox and Moore 1993). Specific adaptations, such as

seed parachutes, are necessary for plants to disperse across

large bodies of water. Such dispersal invokes survival of a

sweepstakes route, an extensive barrier permitting only a

Figure 2—The equilibrium model of species present

on a single island. The equilibrium number of species

is reached at the point of intersection between the rate

of immigration and the rate of extinction (MacArthur

and Wilson 1967).

Figure 3—The equilibrium models of species of several

different islands with a various degrees of isolation and

size. An increase in isolation (near to far) decreases the

immigration curve, while an increase in area (small to

large) decreases the extinction curve (MacArthur and

Wilson 1967).

Figure 4—The correlation between species number, S,

and island area, A, for reptiles and amphibians of the

West Indies. Both axes are logarithmic and a best-fit line

is used. The inset represents this relationship arithmetically (Brown and Lomolino 1998).
166 USDA Forest Service Proceedings RMRS-P-21. 2001

Yu and Lei Equilibrium Theory of Island Biogeography: A Review

stochastic set of immigrants to successfully colonize the

island (Brown and Lomolino 1998). The more remote the

island is from a continental landmass, the more severe the

sweepstakes route and the smaller the number of species

that would successfully colonize and become established on

the island. This is known as the species-isolation relationship on islands. The number of species would decrease

exponentially as a function of isolation because the speciesisolation correlation should account for a pool of species

(fig. 5) (Brown and Lomolino 1998). Successful colonization

over large bodies of water is potentially easier for plants

than for animals. Many species of plants possess dispersal

mechanisms, such as “parachutes and “wings,” to allow new

generations of plants to be carried far from the parent plant

by wind currents. Without having a mate to reproduce,

plants only require one fertile seed or spore to colonize a

remote island. Other mechanisms, such as sticky seeds,

permit seeds to be transplanted by animals. Through animal

assistance, the chance for successful plant immigration is

greatly enhanced. In addition, some plants are able to

withstand long periods of seawater immersion, and successfully colonize remote islands. Such adaptive characteristics

are essential in creating plant communities on both nearby

and remote islands.

Species Turnover

Species turnover on islands is also critical to the ETIB

model. The cycle of extinction of certain established species

and the immigration of new species permit the equilibrium

point to maintain its value over geological time. Such

species turnover, however, can be extremely difficult to

quantify in the field. Whittaker (1998) detects two main

problems with quantifying extinction and immigration rates

on islands. Firstly, species turnover is a situation in which

surveys on islands are at irregular intervals. This phenomenon allows for some species to become extinct and possibly

re-migrate during periods between the surveys, resulting in

a depression of turnover rates (Simberloff 1976). Secondly,

there is potential for pseudoturnover on islands, implying

that information with regard to breeding conditions is

fragmentary or incomplete. Under such circumstances, species appear to have turned over when, in fact, they have

simply been overlooked. With such potential inaccuracies,

the ETIB requires an extensive attention to census detail,

causing it to be a relatively difficult theory to prove under

natural island conditions.

ETIB Strength and Weaknesses

In addition to the limitations in detecting species turnover, Brown and Lomolino (1998) note a number of major

weaknesses in the theory initially proposed by MacArthur

and Wilson. First, many island species rarely achieve equilibrium. The number of species at the equilibrium point may

change over geological time, especially when immigration

and extinction coincide with periods of anomalous climatic

and geological (disturbance) events. Second, not all species

have identical immigration and extinction rates. For instance, birds generally have a higher immigration rate than

large, heavy reptiles and mammals. Third, the ETIB model

regards immigration and extinction as being independent

variables when, in many cases, they are closely related. For

example, when there is a depression or extinction of a

population on an island, a rescue effect may occur, thus

increasing species numbers once again. Fourth, the model

does not consider specific characteristics of species, such as

species fitness and dispersal ability. Fifth, species inhabiting a single island may be derived from several mainland

and island sources. It may be challenging to determine the

source pool for a species on an island without a comprehensive study on the historical and current distribution of the

species. Sixth, the ETIB model does not incorporate speciation, which may exceed immigration rates as a potential

mechanism affecting an island system. Species present by

speciation do not add to the overall species diversity of the

island. This model should include the effects of both speciation and immigration. Seventh, anthropogenic-induced

habitat fragmentation or destruction may isolate once massive and continuous ecosystems on an island. Eighth, the

ETIB model does not consider periodic rescue effect and

target area effect. The rescue effect reduces species extinction, while the target area effect enhances immigration on

large islands. Finally, the use of island size is extremely

general and does not consider the impact of habitat heterogeneity (complexity of habitats and natural landscapes) on

species diversity.

These main arguments against the ETIB are important to

examine. However, modifications of the ETIB are a possibility to account for such problems. Despite such flaws, the

ETIB is still acceptable by some modern scientists in at least

three ways. Firstly, the theory may be graphically simplified, and makes logical sense to a wide array of audiences.

Secondly, this theory forms a link between traditional notions of ecology and biogeography, thereby enriching the

information of both types of study. And, thirdly, this theory

provides a clear and testable strategy for population pattern

predictions not only on islands, but also on localized continental systems.

Figure 5—Display of a negative relationship between

species richness (S) and island isolation (I). The inset

represents the log-transformed equivalent of this relationship (Brown and Lomolino 1998).
USDA Forest Service Proceedings RMRS-P-21. 2001 167

Equilibrium Theory of Island Biogeography: A Review Yu and Lei

Island Conservation _____________

The initial objective for the ETIB was to gain a better

understanding of island ecosystems and their dynamic processes. Nevertheless, as studies continued, many ecologists,

biogeographers, and conservation biologists discovered a

parallel between oceanic islands and fragmented habitats

on continental landmasses. Most species have a range of

habitat in which they prefer to live, yet it has become evident

that human activities such as deforestation, habitat destruction, and urban and suburban development, have all

contributed to a significant fragmentation of natural habitats. The continuation of such fragmentation has resulted in

species extinction from local to global scales (Whitmore and

Sayer 1992). The remaining patches of these relatively

natural areas may be perceived as habitat islands (fig. 6).

From the similarities between habitat islands and actual

oceanic islands, biogeographers utilize the ETIB as a guideline to preserve biodiversity in these patches (Whittaker

1998). This notion, ironically, spawned a great controversy

in the field of biogeography and conservation biology. Janzen

(1983) argues that natural habitats such as parks and

nature preserves vary significantly from true oceanic islands, and thus the ETIB would not be completely applied to

continental reserves. Unlike continental parks, Janzen (1983)

points out that islands are encompassed by water, an extremely different type of habitat. Habitat islands can be

surrounded by a landscape containing a variety of species

that are potentially capable of establishing populations

within the habitat patch. This event often introduces negative biotic interactions, such as competition, predation, and

parasitism, within the habitat island that is not experienced

by true oceanic island ecosystems. Likewise, species within

the habitat island are capable of escaping the patch and

influencing populations of species within the degraded or

fragmented landscape. These are important biotic interactions that do not occur on oceanic islands, and must be

considered when attempting to apply theories of island

biogeography to habitat islands on continents. The scale and

degree of insularity are critical components when making

such comparisons. For these reasons, in addition to theories

concerning oceanic island biogeography, issues such as minimum viable population and area, along with metapopulation

dynamics must be evaluated when determining the most

effective continental reserve design.

Minimum Viable Population and Minimum

Viable Area

The study of population dynamics of a species is critical

when attempting to support the future success of the

species’ population. When evaluating populations of species inhabiting a reserve, survival pressures on these populations are compounded. Smaller areas tend to support

smaller numbers of species as noted by the species-area

concept. Consequently, the proposal of the minimum viable

population (MVP) concept emerged. Shaffer (1981) tentatively defines the minimum viable population for a given

species in a given habitat regardless of the impacts of

demographic stochasticity, environmental stochasticity,

genetic stochasticity, and natural catastrophes. Under this

definition, the survival of the species must not only endure

normal conditions, but also endure episodic catastrophes in

order to persist through geological time.

Shaffer (1981) attempts to give a definitive measure in order

to conserve species living within a restricted area because this

would allow conservation biologists to have a framework in

which to proceed. However, Thomas (1990) argues that the

MVP theory is not realistic with regard to actual population

dynamics within a limited geographical range. Additionally,

Thomas (1990) states that in certain large-scale, remote areas,

the MVP concept would be too difficult to quantify due to the

paucity of available information.

The theory of minimum viable area (MVA) resembles the

theory of minimum viable population. If a determined area

of minimum size is conserved, the species inhabiting such

area is conserved as well. The MVA often corresponds to the

range size in which this particular species is found. Species

located higher on the trophic level generally require more

area or space to ensure maximum survival. Hence, for

certain species, the MVA is considerably large in order for a

MVP to persist within the designated area (Whittaker 1998).

The MVA approach may be effective to help preserve

entire ecosystems since various species coexist and interact

closely within the MVA. However, this concept assumes that

each area is discrete, and has no biotic (genetic) exchange

with other surrounding areas. The MVA must account for

the immigration and colonization of species in and out of the

area (Whittaker 1998). Consequently, the MVA is difficult to

quantify due to its extremely dynamic nature.

Figure 6—The fragmentation of forested land in Cadiz

Township Green County, Wisconsin (94.93 km2), into

habitat “islands” during the era of European settlement

(Shafer 1990).
168 USDA Forest Service Proceedings RMRS-P-21. 2001

Yu and Lei Equilibrium Theory of Island Biogeography: A Review

Metapopulation Dynamics

Metapopulation models first emerged in 1969, and have

since evolved into a dynamic concept involving wildlife

conservation and population turnover. A metapopulation is

a discontinuous distribution of a population of species. This

population is geographically spread over disjunct fragments

of suitable habitat separated by intermixed fragments of

unsuitable habitat through which little migration occurs

(McCullough 1996). As a result, there is a limited movement

of population among suitable patches, and populations remain spatially separated. However, when a metapopulation

becomes environmentally and physiologically stressed, the

population crashes; the patch may be recolonized by a

nearby metapopulation, and may eventually bring the population back up to threshold (fig. 7). Therefore, although

populations of the same species are spatially separated,

migration and gene flow still occur among suitable patches

to ensure long-term survival of the species (Whittaker 1998).

Gotelli (1991) realizes two main dilemmas in studying

metapopulation models. Firstly, the dynamics of metapopulations may be difficult to replicate, especially when

considering the temporal-scale in which metapopulation

changes may occur under natural settings. Secondly, the

subdivision of populations may occur at many levels, and the

degree of separation in metapopulations is often subjective.

Despite potential weaknesses as suggested by Haila (1990),

the metapopulation concept forms a link between population ecology studies and island biogeography theory. Metapopulation models are comprised of dynamic, interdependent

island systems in which population fluctuations are determined by the degree of isolation (Gotelli 1991; Whittaker

1998). These geographically distinct metapopulations may

be viewed as habitat islands due to an extensive human

colonization and development (McCullough 1996). Such

metapopulation pattern is evident in both population ecology and island biogeography studies. Hence, the research

used for island biogeography study may allow for the postulation of a unified concept concerning isolation, area, and

species number on mainland metapopulation systems

(McCullough 1996). However, the application of island biogeography theory to the patch dynamics of metapopulations

has many flaws. Most importantly, habitat patches on a

continental landscape rarely, if ever, resemble true oceanic

islands. Ecotones and edge effects tend to be less dramatic

gradients of habitat than distinct changes from terrestrial

landscapes to seascapes. This dissimilarity introduces two

additional differences between these seemingly analogous

habitats. First, the surrounding area represents a gradient

of habitat, rather than a distinct boundary. The surrounding

habitat may simultaneously offer both advantages, such as

additional food sources, and disadvantages, such as competitors, predators, and pathogens. Second, through properly designed corridors, the surrounding matrix permits

periodic migrations among suitable patches; the degree of

spatial isolation is considerably less on habitat islands than

on true oceanic islands.

Continental Reserve Design and the

SLOSS Debate

Metapopulation dynamic theory is utilized to find the

most effective and efficient strategies for continental reserve design, and has allowed for a better understanding of

population ecology. Many opinions exist concerning the

most effective and “natural” design theory, the size and

shape of reserves, and the number of reserves necessary to

maintain the optimum amount of biodiversity. The SLOSS

debate (Single Large or Several Small) emerged in 1976, and

proposed two schools of thoughts regarding reserve design.

One extreme option was to create a single large reserve. The

other option was to create several small reserves that,

combined, would equal the same area as the large reserve.

Diamond (1981) supports large reserves, using managerial

considerations as a main determining factor. Nilsson (1978)

is also in favor of large reserves, using field data on plant and

bird observations as support. Conversely, Simberloff and

Gotelli (1984) argue that several small reserves would maximize local biodiversity. Shafer (1990) and Simberloff and

Gotelli (1984) utilize plant data to reveal that small reserves

are as effective as a large reserve in maintaining biodiversity.

Like true oceanic islands, a higher degree of isolation on

continental reserves would result in decreased migration

levels to and from the reserve. Furthermore, the destruction

and degradation of habitat surrounding the reserve would

increase extinction rates, as habitat becomes unsuitable to

sustain high biodiversity. A new equilibrium number would

be reached as suitable habitats become less available (fig. 8).

While the reserve is being properly designed and developed,

supersaturation may result primarily due to an excess of

species as displaced populations flee into the still relatively

pristine reserve system. The reserve may not have the

capacity to sustain such high biodiversity, and relaxation

of species numbers into a new point of equilibrium may

eventually occur (fig. 8). The new equilibrium number may

be estimated after information regarding area and degree of

isolation is gathered. Diamond and May (1981) use the

equilibrium point from ETIB to determine what type of

reserve would maximize the species richness and abundance. Whittaker (1998) postulates that larger reserves are

Figure 7—The classic metapopulation model in which

occupied patches (shaded) will re-supply patches in which

the population has decreased or vanished (unshaded).

Movement is denoted by the arrows (Whittaker 1998).
USDA Forest Service Proceedings RMRS-P-21. 2001 169

Equilibrium Theory of Island Biogeography: A Review Yu and Lei

Figure 9—The simplified geometric principles for nature

reserve designs derived from island biogeography research

(Diamond 1975; Whittaker 1998).

Figure 8—According to the assumptions made by the ETIB,

as reduction in area will cause supersaturation as immigration rates decrease and extinction rates increase. This

causes a “relaxation” into a lower species equilibrium point.

Under extreme circumstances, “biotic collapse” may occur

and the results may be an immigration rate so low that the

equilibrium number is zero.

more effective than smaller reserves, shorter distances between reserves are better than longer distances, circular

shaped reserves are better at maintaining reserve species

than elongated shaped reserves due to a reduction of edge

effects, and corridors connecting large reserves would be

more favorable than without corridors (fig. 9).

The use of island biogeography theory has two main

limitations when applying it to the continental reserve

design. Firstly, the ETIB focuses on overall species richness

of a habitat island by using species-area equations. The

ETIB does not allow for the prediction of species with the

highest probability of becoming extirpated from the remaining patch (Saunders and others 1991; Whitmore and Sayer

1992; Whittaker 1998; Worthen 1996). This approach then

does not permit the investigation of specific species circumstances within the reserve, and may prove harmful if requiring in-depth analysis. Secondly, the ETIB model itself is

flawed. Any application of this concept to the continental

reserve design and conservation policy also contains such

flaws (Whittaker 1998). If the use of this theory is not

meticulously studied on a case-by-case basis, certain flaws

are not only represented in reserve design, but also perhaps

even amplified.

Human Impact on Island

Ecosystems ____________________

The utilization of island biogeography theory in determining the most effective reserve design has recently been an

important issue in conservation. Yet, islands themselves

have also been an issue in conservation biology, mainly due

to detrimental human impacts in island environments.

There are numerous heated debates as to what type of

impact the earliest human colonizers had on island ecosystems. Some ecologists and biogeographers argue that most

of the earliest island colonizers were respectful of the island

ecosystem, and that negative impacts occurred only after

secondary arrivals of colonizers conflicted with the interests

of the initial inhabitants. Others argue that earliest inhabitants of some islands devastated the environment because

of their ignorance and negligence concerning island ecosystems. One rather undisputed fact is that as human communities on islands reached the carrying capacity, humans

often modified island landscapes to support the rapidly

growing population. A classic example is the terracing of

steep terrain on islands in order to maximize agricultural

productivity (Nunn 1994). Through history and into the

modern age, negative anthropogenic impacts have continued and increased. Humans can easily damage pristine

island environments in four ways: overexploitation and

predation by humans, habitat loss, fragmentation, and degradation, as well as introduction of exotic species and diseases (biological invasions).

Overexploitation and Predation

by Humans

Many islands contain unique endemic species because the

remote quality of islands allows for the speciation of flora

and fauna to be considerably different from mainland taxa.

A classic example of predation of island species by humans

is that of the dodo bird (Raphus cucullatus), once populated

on the island of Mauritius, located east of Madagascar in the

Indian Ocean. Dodo birds were endemic and were highly

adapted to island conditions. By the early 17th century,

Dutch settlers began to colonize the island, hunting both

dodo birds and tortoises as food sources. Dodo birds became

extinct by the year 1690. Predation of species by humans not

only occurred for food sources, but also for tribal (in other

words, vibrantly colored bird feathers) and exportation reasons. Moreover, fruit bats are currently being exported from

the Polynesian islands. Not only is the declining population

of fruit bats an issue of conservation, but also these bats play

an imperative role in pollination and seed dispersal of island
170 USDA Forest Service Proceedings RMRS-P-21. 2001

Yu and Lei Equilibrium Theory of Island Biogeography: A Review

flora. Therefore, the absence of fruit bat population can also

harm the proliferation of many plant species (Whittaker

1998). A secondary extinction can occur under extreme

cases.

Habitat Loss, Fragmentation, and

Degradation on Island Systems

For centuries, island ecosystems have been the target for

habitat loss, fragmentation, and degradation primarily for

agricultural reasons. In addition, the wood from the forested

trees was used for fuel and residential cooking (Heywood

1979). Such habitat destruction not only directly damages

the island flora, but also reduces the faunal biodiversity. As

forested areas are diminished, suitable habitats and food

resources for fauna also diminish. As habitat fragmentation

(deforestation) continues at an alarming rate, it creates

major ecological dilemmas on islands such as Madagascar.

Another mechanism of habitat degradation or simplification is human-induced fires. Fires are often utilized for

hunting purposes or to clear a plot for agricultural purposes.

Frequent fires in areas with a low natural fire frequency can

be tremendously destructive. Such prescribed burning can

clearly destroy the present island ecosystem and permanently transform the island landscape.

Impact of Exotic Species and Associated

Diseases on Island Ecosystems

As humans travel the globe, different species have been

intentionally and inadvertently introduced into new ecosystems. Many island species, also known as the native biota,

are particularly vulnerable to biological invasions due to

their isolation through evolutionary time. The absence of

herbivory, for instance, has resulted in the persistence of

many island flora with no defensive mechanisms against

grazing pressures. Isolation, in a sense, has protected such

plant species that, otherwise, would have become extinct on

the mainland (Melville 1979). Nevertheless, the presence of

abundant herbivores, such as cattle, sheep, goats, and pigs,

has led to extreme habitat degradation. Historically, humans intentionally introduced these grazing animals to

ensure abundant food supply, without even considering the

negative ecological consequences. However, many of these

animals have become feral and extremely detrimental to the

island landscape. Overgrazing has caused massive erosion

on the hillsides, leading to large-scale landslides. Similarly,

heavy grazing has encouraged the proliferation of exotic

species. The introduction of exotic species into an island

ecosystem is typically irreversible. Some exotic species, in

fact, are more successful in these foreign environments than

in their native landscape. Once those exotic species have

established, their populations rapidly proliferate, making it

nearly impossible to completely extirpate them from the

island.

Foreign diseases on islands are closely associated with

biological invasions onto islands. An exotic species is frequently infected with a disease, and can introduce additional harmful diseases onto the island. If island biota is

immune to the ill effects of the disease, there is little or no

negative impact on the native biota. Conversely, if native

island biota is susceptible to foreign diseases, the results can

be disastrous. The entire island biota is adversely affected,

and many species can be extinguished from the island. If this

species is endemic with a narrow geographic range, the

entire population of this species is likely to become extinct.

Conclusions and Implications _____

This article re-examines the equilibrium theory of island

biogeography initially proposed by MacArthur and Wilson

in 1963. Island environments including topographic origins

and characteristics, along with climatic patterns have been

discussed. The ETIB is analyzed using essential components, such as species-area relationship, island isolation,

dispersal mechanisms, and species turnover. The strengths

and weaknesses of the ETIB model are evaluated. Additionally, continental conservation theories that apply the ETIB

concept are assessed in terms of minimum viable populations and areas, metapopulation dynamics, continental

reserve design, and the SLOSS debate. Lastly, adverse

anthropogenic impacts on island ecosystems, such as

overexploitation of resources, habitat destruction, and introduction of exotic species and diseases, are examined. This

article has primarily re-investigated the research performed

by ecologists, biogeographers, and conservation biologists at

the forefront of island study. The ETIB has been an issue of

heated debate since its emergence nearly four decades ago,

and still today, the vitality of the concepts is evolving as

researchers gain better understanding of island ecosystems

and their pertinence to mainland habitats. This trend will

undisputedly continue, but hopefully researchers will be

able to unlock all of the knowledge to be gained by these

delicate ecosystems before they become relics of the past.

References _____________________

Brown, J.; Lomolino, M. 998. Biogeography (2nd edition). Sunderland,

MA: Sinauer Associates, Inc. 691 p.

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Publications. 244 p.

Dexter, R. W. 1978. Some historical notes on Louis Agassiz’s lecture

on zoogeography. Journal of Biogeography 5:207–209.

Diamond, J. M. 1975. The island dilemma: lessons of modern

biogeographic studies for the design of natural preserves. Biological Conservation 7:129–146.

Diamond, J. M.; May, R. M. 1981. Island biogeography and the

design of nature reserves. Theoretical Ecology (2nd edition).

Oxford, U.K.: Blackwell Scientific Publications.

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propagule rain, and the core-satellite hypothesis. The American

Naturalist 138:768–776.

Haila, Y. 1990. Towards and ecological definition of an island: a

northwest European perspective. Journal of Biogeography

17:561–568.

Heywood, V. H. 1979. The future of island floras. In: Bramwell, D.,

ed. Plants and islands. San Diego, CA: Academic Press. 459 p.

Janzen, D. H. 1983. No park is an island: increase in interference

from outside as park size decreases. Oikos 41:402–410.

Lack, D. 1976. Island biology illustrated by the land birds of

Jamaica. Oxford, U.K.: Blackwell Scientific Publications. 445 p.

Leuschner, C. 1996. Timber line and alpine vegetation on the

tropical and warm-temperate oceanic islands of the world: elevation, structure, and floristics. Vegetatio 123:193–206.
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Equilibrium Theory of Island Biogeography: A Review Yu and Lei

MacArthur, R. H.; Wilson, E. O. 1967. The theory of island biogeography. Princeton, NJ: Princeton University Press. 203 p.

McCullough, D. R. 1996. Metapopulations and wildlife conservation. Washington, D.C.: Island Press. 429 p.

Melville, R. 1979. Endangered island floras. In: Bramwell, D., ed.

Plants and islands. San Diego, CA: Academic Press. 459 p.

Nissan, S. G. 1978. Fragmented habitats, species richness, and

conservation practice. Ambio 7:26–27.

Nunn, P. D. 1994. Oceanic islands. Oxford, U.K.: Blackwell Scientific Publications. 413 p.

Shafer, C. L. 1990. Nature reserves: island theory conservation

practice. Washington, D.C: Smithsonian Institution. 189 p.

Shaffer, M.L. 1981. Minimum population sizes for species conservation. BioScience 31:131–134.

Simberloff, D. 1976. Species turnover and equilibrium island biogeography. Science 194: 572–578.

Simberloff, D.; Gotelli, N. 1984. Effects of insularization on plant

species richness in the prairie-forest ecotone. Biological Conservation 29:27–46.

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species extinction. London, U.K.: Chapman and Hall.

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172 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Simon A. Lei is a Biology and Ecology Professor at the Community College

of Southern Nevada, 6375 West Charleston Boulevard, WDB, Las Vegas,

Nevada 89146-1139.

Abstract—Vegetation response to various types of disturbances

was quantitatively investigated in the Larrea tridentata-Ambrosia

dumosa (creosote bush-white bursage) and Coleogyne ramosissima

(blackbrush) shrublands of southern Nevada. Between the two

control (undisturbed) habitats, the Larrea-Ambrosia vegetation

zone had a greater plant species richness, but had a lower percent

vegetation cover than the Coleogyne zone. Mean plant species

richness and percent vegetation cover were significantly reduced in

edge (disturbed) habitats compared to adjacent undisturbed habitats in both vegetation zones. A major shift in species composition

to favor weedy (pioneer) species was observed in all disturbed

habitats. Mean ratios of weedy to nonweedy species were significantly higher in disturbed relative to undisturbed habitats. Among

the heavily disturbed habitats, roadside corridors exhibited the

greatest, while human trail corridors exhibited the least invasion of

weedy species. Woody and succulent (climax) species are highly

vulnerable to habitat destruction and fragmentation as a result of

natural and anthropogenic disturbances in the Larrea-Ambrosia

and Coleogyne vegetation zones of southern Nevada.

Introduction ____________________

Habitat alteration and destruction are direct habitat

removal when an ecosystem is converted to residential,

recreational, commercial, agricultural, and industrial areas. Habitat destruction and fragmentation typically begin

with gap formation or perforation of the vegetation matrix as

humans colonize a Mojave Desert landscape or begin extracting resources there (Lord and Norton 1991; Meffe and

Carroll 1997). As the gaps get bigger and more numerous,

the original Mojave Desert woody vegetation is broken.

Roads and powerline corridors as narrow as 8 m may

produce significant edge effects by attracting weedy and

exotic plant species (Meffe and Carroll 1997). Habitat destruction, fragmentation, and degradation can alter species

richness initially, but often favors weedy and exotic species.

Metapopulation dynamics suggest that even once common

native desert plant species are not completely immune to the

adverse effects of widespread habitat fragmentation and

degradation (Brown and Lomolino 1998; Meffe and Carroll

1997; Noss 1983). Weedy plants are initially found along the

edges, and these plants can become well established in

Vegetation Response to Natural and

Anthropogenic Disturbances in the LarreaAmbrosia and Coleogyne Shrublands

Simon A. Lei

desert interiors and outcompete natives at certain areas

through time (Lei, personal observation 1998).

The internal fragmentation of once pristine natural areas by

roads, trails, powerlines, fences, and other anthropogenic activities has not been well studied, but it has potentially dramatic effects on native biodiversity (Meffe and Carroll 1997).

The Las Vegas Valley and vicinity have experienced a rapid

urbanization, economic growth, and recreational activities in

recent years. Yet, a comparative vegetation response to various natural (fire and soil erosion) and anthropogenic (human/

jeep trail, roadside, powerline, fence, and construction site)

disturbances remain poorly understood. The objectives of this

article were to compare changes in plant species richness,

percent vegetation cover, and weedy/nonweedy species ratio

among edge (disturbed) habitats of the Larrea-Ambrosia and

Coleogyne vegetation zones in Las Vegas and the adjacent

Spring Mountains of southern Nevada.

Methods _______________________

Study Site

Field studies were conducted in the Las Vegas Valley

and the adjacent Spring Mountains (roughly 36°30' N,

115°30' W; fig. 1) in southern Nevada during Fall 1998.

Figure 1—A sketch map showing location of study

sites in southern Nevada. The Spring Mountains

lie just to the west of the Las Vegas Valley.
USDA Forest Service Proceedings RMRS-P-21. 2001 173

Vegetation Response to Natural and Anthropogenic Disturbances in the Larrea-Ambrosia and Coleogyne Shrublands Lei

The Larrea-Ambrosia vegetation zones occur at low elevations of the Las Vegas Valley, while the Coleogyne zones

occur directly above the Larrea-Ambrosia zones at midelevations of the Spring Mountains.

The natural Mojave Desert woody vegetation occurred

throughout the Las Vegas Valley and the Spring Mountains

several centuries ago (fig. 2A). Gaps were gradually formed

several decades ago, but became highly intensified in recent years as humans rapidly colonize this desert landscape (figs. 2B-C). At the present time, a substantial portion

of the natural desert vegetation is broken (fig. 2D). Considerably more habitat destruction through fragmentation is

expected in the near future due to rapid urbanization

through residential, recreational, commercial, and industrial (economic) development. Eventually, the Las Vegas

Valley and vicinity will become an immense anthropogenic

habitat, with relatively little remaining of the native Mojave

Desert woody vegetation.

The four seasons are well defined. Summers display desert

conditions, with a maximum air temperature usually in the

40 °C range. Winters are generally mild and pleasant, with

a minimum temperature just below the freezing range

(Local Climatological Data, Las Vegas). The spring and fall

seasons are considered most ideal, although sharp temperature changes can occur during these months. The precipitation patterns include summer storms and winter rains.

Summer rainfalls generally occur in July through early

September, and come from the Gulf of California, drawn

into the Mojave Desert by strong convectional currents

(Rowlands and others 1977). Conversely, winter rains are

mild and widespread, and come from the Pacific Ocean.

Winter rainfalls may last several days. Winter and summer

precipitation contribute significantly to the annual precipitation (table 1), which varies considerably from year to year.

Figure 2—A schematic diagram showing a temporal

sequence of habitat destruction through fragmentation

starting from an original Mojave Desert woody vegetation (A) to a massive anthropogenic habitat (D).

Table 1—Mean monthly precipitation and mean monthly maximum

and minimum air temperature based on the 1936-1997

data in the Las Vegas Valley. The climatological data

(National Weather Service) were obtained collectively

from multiple long-term weather stations in Las Vegas of

southern Nevada.

Air temperature (°C)

Month High Low Precipitation (mm)

January 14.4 1.1 12.7

February 17.2 3.9 11.4

March 20.6 6.7 10.2

April 25.6 10.6 5.1

May 31.1 15.6 5.1

June 37.7 20.6 5.1

July 41.1 23.3 11.4

August 39.4 23.3 14.0

September 35.0 18.9 7.6

October 27.8 12.2 6.4

November 19.4 6.1 11.4

December 14.4 1.1 7.6

In general, precipitation is positively correlated with

elevation (Rowlands and others 1977). Relative humidity

of 20 percent or less is common in the summer months,

resulting in exceedingly high evaporation (Lei and Walker

1997a,b).

Field Surveys and Statistical Analyses

Three transects were established along each of the eight

types of natural and anthropogenic disturbances (a total of

24 transects) in the Larrea-Ambrosia and Coleogyne vegetation zones. Three transects were also established in the

adjacent undisturbed (control) habitats in each of the two

vegetation zones. Each transect was 400 m in length. Within

each transect, 10 (20 x 20 m) plots were randomly placed to

avoid biased vegetation sampling. Within each plot, species

richness was quantified, and vegetation cover was visually

quantified in 10 percent increments. Ratios of weedy to

nonweedy species were also computed.

Within each type of disturbance, vegetation data from

three transects were pooled. One-way Analysis of Variance

(ANOVA; Analytical Software 1994) was conducted to detect

differences in vegetation attributes among the eight types of

disturbed habitats in the Larrea-Ambrosia and Coleogyne

shrublands. Tukey’s Multiple Comparison Test (Analytical

Software 1994) was performed to compare mean species

richness, percent vegetation cover, and ratio of weedy to

nonweedy species when a significant habitat effect was

detected. Mean values are expressed with standard errors,

and statistical significance is determined at p ≤ 0.05.

Results ________________________

The Larrea-Ambrosia vegetation zone was considerably

more disturbed and fragmented by anthropogenic activities than the Coleogyne zone in recent years in southern

Nevada. Mean species richness declined significantly (p ≤

0.001; fig. 3) across the six types of disturbed habitats
174 USDA Forest Service Proceedings RMRS-P-21. 2001

Lei Vegetation Response to Natural and Anthropogenic Disturbances in the Larrea-Ambrosia and Coleogyne Shrublands

compared to adjacent undisturbed habitats in the LarreaAmbrosia vegetation zone. Among the edge habitats, roadside corridors had the greatest, while fence corridors had the

lowest mean species richness (fig. 3). Mean percent vegetation cover also decreased significantly (p ≤ 0.001; fig. 4) in

these disturbed habitats relative to undisturbed habitats.

Figure 3—Species richness (mean ± S.E., n =

30 plots in each type of disturbance) in disturbed and undisturbed (control) habitats in the

Larrea-Ambrosia shrublands. Symbols of disturbed habitats: Control (CT); jeep trail (JT);

roadside (RS); Powerline (PL); construction

site (CS); fence (FE); and gully erosion (GE).

Figure 4—Percent vegetation cover (mean ± S.E., n =

30 plots) in disturbed and undisturbed (control) habitats

in the Larrea-Ambrosia shrublands. Symbols of disturbed habitats are explained in figure 3.

Roadside corridors revealed the greatest, whereas gully

erosion corridors revealed the lowest mean percent vegetation cover (fig. 4). However, mean ratio of weedy to nonweedy

species increased significantly (p ≤ 0.001; fig. 5) in disturbed habitats compared to undisturbed habitats in the

Larrea-Ambrosia shrubland. Roadside corridors exhibited

the highest mean ratio with a variety of weedy, herbaceous

species (fig. 5).

Furthermore, mean species richness was significantly

lower (p ≤ 0.001; fig. 6) across the five types of disturbed

habitats compared to adjacent undisturbed habitats in the

Coleogyne shrubland. Conversely, mean species richness

between the roadside and undisturbed habitats did not

differ significantly (fig. 6). Mean percent vegetation cover

was significantly lower (p ≤ 0.001; fig. 7) in disturbed than

undisturbed habitats. Roadside corridors exhibited the greatest, while fence corridors exhibited the lowest mean percent

vegetation cover (fig. 7). In contrast, mean ratio of weedy to

nonweedy species was significantly higher (p ≤ 0.001; fig. 8)

in disturbed relative to undisturbed habitats in the Coleogyne

vegetation zone. Among the highly disturbed habitats, roadside corridors showed the highest mean ratio with abundant

weedy, herbaceous individuals (fig. 8).

Discussion _____________________

The Las Vegas Valley and the Spring Mountains of southern Nevada have recently experienced a severe habitat

destruction through fragmentation largely due to rapid

urbanization, economic growth, and recreational activities.

Ecological impacts of disturbance on vegetation of the LarreaAmbrosia and Coleogyne vegetation zones have been conspicuous. The Mojave Desert habitats disturbed by natural

and anthropogenic forces contributed to significant shifts in

plant species richness, percent vegetation cover, and ratio of

Figure 5—Ratio of weedy to nonweedy species

(mean ± S.E., n = 30 plots) in disturbed and

undisturbed (control) habitats in the Larrea-Ambrosia shrublands. Symbols of disturbed habitats

are explained in figure 3.
USDA Forest Service Proceedings RMRS-P-21. 2001 175

Vegetation Response to Natural and Anthropogenic Disturbances in the Larrea-Ambrosia and Coleogyne Shrublands Lei

Figure 6—Species richness (mean ± S.E., n = 30 plots in

each type of disturbance) in disturbed and undisturbed

(control) habitats in the Coleogyne shrublands. Symbols

of disturbed habitats: Control (CT); human trail (HT); jeep

trail (JT); roadside (RS); fire (FI); and fence (FE).

Figure 8—Ratio of weedy to nonweedy species (mean

± S.E., n = 30 plots) in disturbed and undisturbed

(control) habitats in the Coleogyne shrublands. Symbols of disturbed habitats are explained in figure 6.

Figure 7—Percent vegetation cover (mean ± S.E., n = 30

plots) in disturbed and undisturbed (control) habitats in

the Coleogyne shrublands. Symbols of disturbed habitats

are explained in figure 6.

weedy to nonweedy species to favor weedy and opportunistic

species.

From casual observations, weedy species, such as Russian

thistle (Salsolakali), Pectispapposa, red brome grass (Bromus

rubens), and Eriogonum spp., colonize within two months

after initial disturbances. In this study, species richness and

percent vegetation cover decreased significantly at highly

disturbed sites, primarily due to the complete or nearly

complete removal of native woody vegetation in the LarreaAmbrosia and Coleogyne zones. Conversely, native woody,

subwoody, and succulent plants contribute substantially to

species richness and percent vegetation cover at undisturbed sites. Disturbance and fragmentation are not isolated events; rather, they are ongoing processes and may

lead to a complete replacement of the native vegetation by

many weedy and exotic plants along the edge habitats (Soule

and others 1992). The ratio of weedy to nonweedy species

was significantly higher at disturbed than undisturbed sites

in this study, and such ratio is often more useful than species

abundance and richness (Meffe and Carroll 1997). In both

Larrea-Ambrosia and Coleogyne vegetation zones, roadside

disturbance exhibited the highest ratio of weedy to nonweedy

species, presumably due to an excess moisture supply (surface water run-off) along the gutter after major storm events.

Nevertheless, human trail disturbance exhibited the lowest

ratio of weedy to nonweedy species since the trails were

typically less than 1.5 m wide and the extent of disturbance

beyond the trails was minimal in this study.
176 USDA Forest Service Proceedings RMRS-P-21. 2001

Lei Vegetation Response to Natural and Anthropogenic Disturbances in the Larrea-Ambrosia and Coleogyne Shrublands

Natural and anthropogenic disturbances through fragmentation in the Larrea-Ambrosia and, to a lesser extent,

Coleogyne shrublands have led to a substantial habitat loss,

and have created edge habitats and spatial heterogeneity.

Edge zones subject to more disturbance than interior core

zones, favoring weedy and opportunistic (edge) species

(Murica 1995; Soule and others 1992). In general, the greater

the structural contrast between adjacent undisturbed habitats, the more intense the edge effects (Meffe and Carroll

1997). The Mojave Desert landscape in Las Vegas has

abundant edge zones and may gradually become dominated

by edge-adapted species. The edge effect studies suggest

that species composition and abundance patterns change in

disturbed landscapes because some species are more vulnerable than others to increased isolation (metapopulation),

edge effects, reduced interior core areas that contain critical

resources, and other factors that accompany the disturbance

process (Meffe and Carroll 1997; Murica 1995). As cosmopolitan plant species invade more and more disturbed areas,

local vegetation types are likely to become homogenized by

losing their floristic and ecological distinctness through

time.

Implications and Future

Directions______________________

Habitat destruction and fragmentation are a major threat

to biodiversity without significant changes in climatic,

edaphic, and geomorphic conditions. Significant alterations

in species diversity and vegetation cover at a local scale due

to invasions by weedy and exotic species were evident in the

Las Vegas Valley and vicinity. Although not quantitatively

investigated in this study, biotic interactions, along with

ecological processes and attributes, may change substantially as a result of edge effects and other accompaniments

of habitat destruction and fragmentation. As urbanization,

economic growth, and recreational activities intensify

through time, considerably more conversion of a native

Mojave Desert woody vegetation to an immense anthropogenic habitat is fully expected. Landscape restoration and

large-scale revegetation to the original, pristine level are

virtually impossible. In recognition of the alarming yet

largely unmeasured destruction and conversion of native

desert habitats, future research is required to properly

address the biological underpinnings of ecological and conservation issues. Such issues may include ecological processes and attributes, biotic interactions, biodiversity, invasive and endangered species, metapopulation dynamics, as

well as reserve size and design in a fragmented landscape

caused by natural and anthropogenic disturbances in the

southern Nevada region of the Mojave Desert.

Acknowledgments ______________

I gratefully acknowledge Steven Lei, David Valenzuela,

and Shevaun Valenzuela for providing valuable field assistance. I also sincerely appreciate the Department of Biology

at the Community College of Southern Nevada (CCSN) for

providing logistical support.

References _____________________

Brown, J.H.; Lomolino, M.V. 1998. Biogeography. Sunderland, MA:

Sinauer Associates, Inc. 691 p.

Lei, S.A.; Walker, L.R. 1997a. Classification and ordination of

Coleogyne communities in southern Nevada. Great Basin Naturalist 57:155–162.

Lei, S.A.; Walker, L.R. 1997b. Biotic and abiotic factors influencing

the distribution of Coleogyne communities in southern Nevada.

Great Basin Naturalist 57:163–171.

Lord, J.M.; Norton, D.A. 1990. Scale and the spatial concept of

fragmentation. Conservation Biology 4:197–202.

Meffe, G.K.; Carroll, C.R. 1997. Principles of Conservation Biology.

Sunderland, MA: Sinauer Associates, Inc. 729 p.

Murica, C. 1995. Edge effects in fragmented forests: Implications for

conservation. Trends in Ecology and Evolution 10:58–62.

Noss, R.F. 1983. A regional landscape approach to maintain

biodiversity. Bioscience 33:700–706.

Rowland, P.G.; Johnson, H; Ritter, E.; Endo, A. 1977. The Mojave

Desert. In: M. Barbour and J. Major, editors, Terrestrial vegetation of California. John Wiley and Sons, New York. 1002 p.

Soule, M.E.; Alberts, A.C.; Bolger, D.T. 1992. The effects of

habitat fragmentation on chaparral plants and vertebrates.

Oikos 63:39–47.
USDA Forest Service Proceedings RMRS-P-21. 2001 177

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Jeffrey E. Ott is a Biological Technician, U. S. Department of Agriculture,

Forest Service, Rocky Mountain Research Station, Shrub Sciences Laboratory, and an M.S. candidate, Brigham Young University, Department of

Botany and Range Science, Provo, UT. E. Durant McArthur is Project Leader

and Supervisory Research Geneticist, Stewart C. Sanderson is Research

Geneticist, U. S. Department of Agriculture, Forest Service, Rocky Mountain

Research Station, Shrub Sciences Laboratory, Provo, UT.

Plant Community Dynamics of Burned and

Unburned Sagebrush and Pinyon-Juniper

Vegetation in West-Central Utah

Jeffrey E. Ott

E. Durant McArthur

Stewart C. Sanderson

Abstract—Fire ecology of sagebrush and pinyon-juniper vegetation in the Great Basin has been influenced by human disturbances

and exotic plant introductions. Late-seral woody vegetation, which

increased following Euro-American settlement, is now decreasing

because of wildfire and exotic annuals. Multiple successional pathways following fire have been observed in these vegetation types.

Following the 1996 wildfires in west-central Utah, burned and

unburned vegetation were compared at four sites. Measures of

frequency, cover, and density of vascular plant species were used to

show fire effects and to follow population dynamics over a period of

3 years. Woody species characteristic of the unburned areas were

generally absent from the burned areas. Native herbaceous species,

particularly annual forbs, were abundant in the burned areas 1 year

after the fires, but many of these declined by the second and third

year, as exotic species, particularly cheatgrass (Bromus tectorum),

increased. Cheatgrass became dominant in the interspaces among

burned trees by the second year following the fires, a period of high

precipitation. In the subcanopy zones of burned trees, cheatgrass

did not become dominant until the third year following the fire, and

was preceded by exotic annual forbs. Community composition and

structure differed by site as well as by fire history. Cheatgrass cover

was lowest at a site where perennial grasses and forbs had become

established through aerial broadcast seeding.

Introduction ____________________

Large portions of the semiarid Great Basin region of Utah,

Nevada, and surrounding states are occupied by vegetation

types that are referred to as sagebrush and pinyon-juniper.

These vegetation types are named for their dominant woody

plant species, including big sagebrush (Artemisia tridentata),

Utah juniper (Juniperus osteosperma), singleleaf pinyon

(Pinus monophylla), and Colorado pinyon (Pinus edulis)

(West 1988). These species occur in association with a

variety of other species of shrubs, grasses, and forbs (Bunting

and others 1999; Rust 1999). The vegetation structure and

floristic composition of sagebrush and pinyon-juniper communities are variable over the wide geographical and ecological ranges of these vegetation types. At some locations,

sagebrush vegetation has historically included a significant

perennial grass component, and is described as sagebrush

steppe (West 1988). Mature pinyon-juniper woodlands often

have sparse herbaceous understory, and are common on

steeper, rockier, and higher elevation sites than sagebrush

vegetation (West 1988; West 1999). At many sites, however,

the distinction between sagebrush and pinyon-juniper is

blurred because either could potentially occur. Pinyonjuniper is capable of invading sagebrush (Miller and Wigland

1994), and sagebrush often occurs in the early successional

stages of pinyon-juniper (Barney and Frischknecht 1974).

Tausch (1999) described shrub and steppe communities as a

matrix within which pinyon-juniper woodlands of various

successional stages are present.

Fire is an important ecological factor in the sagebrush and

pinyon-juniper vegetation types. Estimates of fire return

intervals prior to Euro-American settlement range from 20

to 25 years for the sagebrush steppe of Yellowstone National

Park (Houston 1973) to 50 to 100+ years for the xeric pinyonjuniper woodlands of Great Basin National Park (Gruell

1999). The historical impact of fire has differed by region,

due to differences in factors such as the occurrence of

summer thunderstorms (Billings 1994). In fire-prone areas,

selective pressure has favored plants that are either capable

of surviving fire, or able to occupy the environments of

successional stages that follow fire (Wright and others 1979;

Bradley and others 1992).

Early successional stages following fire are often characterized by herbaceous species, because the primary woody

dominants (big sagebrush, Utah juniper, and pinyon) are

easily killed by fire and require long fire-free periods to

reestablish and mature (Billings 1994; Miller and Wigland

1994). Barney and Frischknecht (1974) described a sequence of successional stages following fire in juniper woodlands of west-central Utah, based on examination of several

burns of different ages. An annual phase lasting 3 to 4 years

was succeeded by a perennial grass/forb stage, which then

gradually became occupied by maturing shrubs and trees.

Sagebrush generally became dominant after 35 years, and

juniper after 70 years. These authors noted that the rate and

character of succession may vary, due to factors such as seed

availability, pre-burn vegetational composition, and grazing. At locations where fire-tolerant perennial species, such

as bluebunch wheatgrass (Elymus spicatus), were abundant

prior to the fire, the annual stage could be shortened or
178 USDA Forest Service Proceedings RMRS-P-21. 2001

Ott, McArthur, and Sanderson Plant Community Dynamics of Burned and Unburned Sagebrush and Pinyon-Juniper Vegetation in West-Central Utah

bypassed. Heavy grazing had the potential to inhibit

perennial grasses and increase the rate of sagebrush establishment (Barney and Frischknecht 1974).

Other successional sequences are also possible because of

widespread disturbances and exotic plant invasions that

have occurred in the sagebrush and pinyon-juniper vegetation types since the time of Euro-American settlement.

Prolonged livestock grazing and fire suppression practices

have contributed to a decline of perennial grasses and an

increase in shrubs and trees at many sites (Tausch and

others 1981; Laycock 1991). Currently, there is a reversal in

this trend, with shrubs and trees being lost as a result of an

increased number of large, high-intensity fires (Tausch

1999). One of the factors contributing to this increase in fire

is the presence of invasive exotic annuals, particularly the

widespread annual cheatgrass (Bromus tectorum) (D’Antonio

and Vitousek 1992). Following fire, cheatgrass readily reestablishes from seed, and alters successional trajectories by

interfering with native plant seedling establishment (Stewart

and Hull 1949) and shortening the interval between fires

(Whisenant 1990). The exotic annual forbs Russian thistle

(Salsola pestifer) and tumblemustard (Sisymbrium

altissimum) often dominate early post-fire successional stages

on disturbed sites where cheatgrass will later become dominant (Piemeisel 1951).

To account for such alternative successional patterns,

state-and-transition models (Westoby and others 1989) have

been applied to the sagebrush and pinyon-juniper vegetation types (Jameson 1987; Laycock 1991). According to the

state-and-transition model of Laycock (1991) for sagebrush

steppe, fire, grazing, and annual invasion can lead to a

threshold beyond which the climax steady state becomes an

annual grassland. After such a threshold has been crossed,

intensive human intervention in the form of weed control

and revegetation treatment may be necessary to restore the

system to its former state, or to an alternative state containing desirable perennial species. Artificial seeding of perennial species such as crested wheatgrass (Agropyron cristatum)

is commonly carried out following wildfire on managed lands

to preclude the development of undesirable cheatgrass stands

and to meet other management objectives (Evans and Young

1978; MacDonald 1999).

During the summer of 1996, several large lightningcaused wildfires occurred in western Utah, burning thousands of acres of sagebrush and pinyon-juniper (MacDonald

1999). The study presented here was carried out following

these fires to document the effect of the fires on plant

community composition and structure, and successional

changes over a period of 3 years. Attention was given to the

distribution and dynamics of individual species, and groups

of species organized according to origin (native or exotic), life

form (grass, forb, shrub, or tree), and longevity (annual or

perennial). This report is part of a broader study of wildfire

rehabilitation following the 1996 fires (Ott 2001).

Study Sites and Methods _________

Four study sites were selected in 1997, at locations in

west-central Utah where wildfires had occurred the previous

year (fig. 1; table 1). The Gilson and Jericho sites were part

the Leamington complex fire, which burned during early

August 1996. The Twin and Cunningham sites represent

separate fire complexes, which burned during early July and

August 1996, respectively (BLM, personal communication).

At each of these sites, unburned vegetation occurred adjacent to burned vegetation of similar composition and structure. The burned portion of the Cunningham site had been

rehabilitated through aerial broadcast seeding during the

fall of 1996 by the Bureau of Land Management. Rehabilitation treatments including aerial seeding, chaining, and

rangeland drill seeding were carried out by the Bureau of

Land Management at the Jericho, Gilson, and Twin sites. In

addition, burned but untreated controls were present at the

foregoing sites on non-BLM lands (highway right-of-ways,

state, and private lands). The data presented in this paper

for the Jericho, Gilson, and Twin sites were collected on

these untreated burned areas.

At each study site, a cadestral survey marker or other

reference point was located, and transect lines were directed

from the reference point into areas of burned and unburned

vegetation, which we refer to as burned and unburned

treatments. Within each treatment/site combination, four

permanent plots were established at tape-measured intervals of 50 m (Twin and Gilson sites) or 60 m (Cunningham

and Jericho sites). A metal rebar was used to mark the center

of a circular plot of area 100 m2 (0.025 acre), and also served

Figure 1—Location of study sites in relation to 1996

wildfire complexes (shading) in west-central Utah.

Jericho

Gilson

Twin

Cunningham
USDA Forest Service Proceedings RMRS-P-21. 2001 179

Plant Community Dynamics of Burned and Unburned Sagebrush and Pinyon-Juniper Vegetation in West-Central Utah Ott, McArthur, and Sanderson

as the southwest corner of a square-shaped 1 m2 plot

(McArthur and Sanderson 1996).

Composition and foliar cover of vascular plant species

were recorded for both plot sizes. Species nomenclature

followed Welsh and others (1993). For the large (100 m2

)

plots, each species present (having canopy within the plot

boundary) was assigned a cover class, based on classes

proposed by Daubenmire (1959), with an additional cover

class added to accommodate species having less than 1 percent cover (McArthur and Sanderson 1996). For the small

(1 m2

) plots, a whole-number percent cover estimate was

made for each species. Total cover of understory plants

(excluding trees), and any bare soil, rock (>1 cm diameter),

litter, or cryptobiotic crust exposed beyond the understory

cover, were also estimated for the small plots. The number

of rooted individuals of each species was also counted for

small plots; counts were rounded to the nearest 5 or 10 when

the number of individuals exceeded 50.

Plot data as described above were collected each year for

3 consecutive years (July to August 1997, June to early July

1998, and late June to early August 1999). In 1998, additional data were collected using a step-point technique

modified from Evans and Love (1957). A step-point transect

consisting of 40 points was extended from the edge of each

large plot along the transect line upon which the plot had

been placed. At paced intervals of 1 m, a pin (2 mm diameter

wire attached to a meterstick) was lowered to the ground

directly in front of the recorder’s boot. Basal cover at the

intersection of the pin and the ground was identified as bare

soil, rock, litter, cryptobiotic crust, or a species of vascular

plant. Litter was defined to include dead wood at ground

level and dead herbaceous material from a previous year.

Tree canopy above each point was also recorded, with canopy

above dead burned trees estimated as if they were foliated.

If a tree or shrub became an obstacle along a transect line,

the line was maintained by extending the meterstick, from

point to point, beneath or through the canopy of the tree or

shrub, then resuming paced steps on the opposite side. If the

boundaries of the treatment area were reached before a

transect line was complete, the direction of the transect was

redirected by 135° to complete the sample within the treatment of concern.

Recorded plant species were variously organized into

groups based on life form (tree, shrub, grass, or forb), origin

(native or exotic), and longevity (perennial or annual), as

indicated by Welsh and others (1993). Species that had been

used in the rehabilitation seedings were also segregated.

Biennial species were considered perennial unless the species also typically grows as an annual. For each of the

resulting groups (native shrubs and trees, native grasses,

exotic grasses, seeded grasses, seeded shrubs and forbs,

exotic forbs, native annual forbs, and native perennial forbs),

synthetic percent-cover values were created by adding the

cover values of all species within the group. Synthetic

percent-cover values for large plots were computed using the

midpoints of cover classes.

Cover data for synthetic species groups were analyzed

statistically using SAS statistical software (SAS Institute,

Inc. 1990). Large and small plots were analyzed separately.

The Cunningham site, which had been aerially seeded, was

excluded from this analysis in order to highlight the response where seeding had not been done. SAS PROC MIXED

was used to run a mixed model, first order autoregressive

repeated measures analysis (Littell and others 1996). Site

and the interaction of site with treatment and year were

treated as random effects, while treatment, year, and their

interaction were treated as fixed effects. The Tukey adjustment was used to test differences between treatment, year,

and treatment by year means. The PROC UNIVARIATE

procedure in SAS was used to test for normality of residuals

(considered normal if the Shapiro-Wilk statistic was greater

than or equal to 0.05). Percentage variables failing to meet

this test of normality were retested following an arcsine

transformation of the square root of the percentage value

(Snedecor 1956).

Other data were examined and used to make comparisons,

but were not analyzed using parametric statistics. Cover

and density of individual species were averaged across the

three nonseeded sites by treatment and year. Frequency,

here defined as the number of plots where a species was

present, was tabulated by year and treatment, across all

sites, for each species. Basal cover, based on the 1998 steppoint transects, was averaged by treatment and site for each

synthetic species group.

Table 1—Description of study sites in west-central Utah where burned and unburned plant communities were sampled following 1996 wildfires.

Site name Location (marker) Elevation Range of slopes Soils Site description

ft percent

Cunningham Rebar at canyon mouth, 6,400–6,500 20–35 Red Butte very Rocky east-facing slopes

T27S R7W S34 S35 S2 T27S rocky loama

Gilson Section marker 5,320–5,400 4–15 Borvant cobbly loamb Eastern foothills of Gilson

T13S R3W S35 T14S R3W S1 S2 Mountains

Jericho Milemarker 124, US Hwy. 6, 5,420–5,480 4–16 Jericho gravelly fine South side of Tintic Valley

T12S R3W S28 sandy loamb

Twin Quarter-section marker 5,900–5,940 1–6 Kessler-Penoyer very Basalt plains

T25S R7W S29 S32 cobbly loama

a

Stott, L. H.; Olsen, M. E. 1976. Soil survey of Beaver-Cove Fort area, Utah. U.S. Department of Agriculture, Soil Conservation Service. b

Trickler, D. L.; Hall, D. T. 1984. Soil survey of Fairfield-Nephi area, Utah. U.S. Department of Agriculture, Soil Conservation Service.
180 USDA Forest Service Proceedings RMRS-P-21. 2001

Ott, McArthur, and Sanderson Plant Community Dynamics of Burned and Unburned Sagebrush and Pinyon-Juniper Vegetation in West-Central Utah

Results and Discussion __________

First-Year Burned/Nonburned Comparison

Species frequencies among sites and years in burned and

unburned treatments are shown in table 2. Some species

were recorded much more frequently in either the burned or

the unburned treatment, while others occurred more uniformly in both treatments or were too rare to reveal differences. Species with the greatest difference in frequency

between burned and unburned large plots in 1997 are

highlighted in table 3. Species with the highest frequency in

burned plots relative to unburned were primarily annual

forbs, including the native species pinnate tansymustard

(Descurainia pinnata), floccose gilia (Gilia inconspicua),

groundsmoke (Gayophytum lasiospermum), whitestem

blazingstar (Mentzelia albicaulis), and coyote tobacco (Nicotiana attenuata); and the exotic species prickly lettuce

(Lactuca serriola), African mustard (Malcolmia africana),

and tumblemustard (Sisymbrium altissimum). Seeded species, not shown in table 3, also had greater frequency in the

burned areas. The species with the highest frequency in the

unburned plots relative to the burned included native trees

and shrubs such as Utah juniper (Juniperus osteosperma),

big sagebrush (Artemisia tridentata), viscid rabbitbrush

(Chrysothamnus viscidiflorus), and native perennial forbs

such as desert phlox (Phlox austromontana) and Holboell’s

rockcress (Arabis holboelii). Species with high frequencies

in both burned and unburned plots, not shown in table 3,

included cheatgrass (Bromus tectorum), bottlebrush

squirreltail (Elymus elymoides), bluegrass (Poa spp.), Indian ricegrass (Stipa hymenoides), bluebunch wheatgrass

(Elymus spicatus), Douglas’ dustymaiden (Chaenactis

douglasii), sego lily (Calochortus nuttallii), longleaf phlox

(Phlox longifolia), and bur buttercup (Ranunculus

testiculatus).

When mean percent cover, based on the cover-class midpoints for the large plots, was used to identify species with

different abundances in the burned and unburned treatments, results were similar to those for frequency, with some

notable exceptions (table 3, right). Cheatgrass (Bromus

tectorum) was present in all plots, burned and unburned, but

its mean percent cover 1 year following the fire was 7.3

percent higher on burned than on unburned plots. The exotic

annual forb desert alyssum (Alyssum desertorum) had higher

frequency in the unburned plots but higher cover in the

burned. The native perennial grasses bottlebrush squirreltail,

muttongrass (Poa fendleriana), and Indian ricegrass also

had higher cover in the unburned plots. Most species had

only slight differences (less than 1 percent) in mean percent

cover between burned and unburned plots.

Although the comparison of plots in adjacent burned and

unburned areas is not as conclusive as would be a comparison of a single set of plots before and after a fire, these results

are nevertheless instructive. We assume that the differences in frequency and cover between the burned and unburned treatments are in large measure due to the effects of

the fires. Perennial species with lower abundance in the

burned treatments likely suffered mortality or direct damage from the fires, or were indirectly affected because they

were better adapted to the late-seral than to the early-seral

environments.

The fires at our study sites were of sufficient intensity to

kill nearly all individuals of nonbase-sprouting perennial

species, including Utah juniper, pinyon, and big sagebrush.

Viscid rabbitbrush also appeared to have been eliminated by

the fires at our study sites, even though the typical response

of this species is vigorous resprouting (Wright and others

1979; Everett and Ward 1984). Zschaechner (1985) observed

mortality of viscid rabbitbrush following fire and suggested

that this was the result of high amounts of fuel in the vicinity

of the plants, which raised the heat load to lethal levels.

Herbaceous perennials with lower abundance in the burned

treatments, such as desert phlox, Holboell’s rockcress, and

bottlebrush squirreltail, may have likewise been damaged

because of the high intensity of the fires. In the unburned

treatments, bottlebrush squirreltail was observed most commonly in the zone beneath juniper trees. Similar concentrations of this species beneath trees prior to the fire in the

burned treatments would have likely suffered high mortality because of the high intensity of fire that typically occurs

in subcanopy zones (Klebenow and others 1977).

The timing of a fire relative to periods of growth and

dormancy is another important variable affecting fire response (Wright and others 1979). Most perennial grasses

encountered in our study were cool-season species, which

were probably less damaged by the late-summer 1996 fires

than they might have been if burned earlier in the growing

season. Residual patches of bluebunch wheatgrass and western wheatgrass (Elymus smithii) were present in the burned

treatment, even at the Twin site, which had burned in early

July.

Many of the native and exotic annual forbs that we

recorded in the burned treatments, including members of

the genera Chenopodium, Collinsia, Descurainia, Gilia,

Lactuca, Mentzelia, Nicotiana, Sisymbrium, Salsola, and

Polygonum, have been reported by other authors studying

early succession following fire in sagebrush and pinyonjuniper areas (Young and Evans 1978; Everett and Ward

1984; Koniak 1985). Seeds of these annuals were either part

of the seedbank that survived the fires, or arrived through

rapid dispersal following the fires. Koniak and Everett

(1982) found that most of the seedbank in a mature pinyonjuniper stand consisted of annuals, many of which were not

present in the community as mature plants. Fire may

promote the germination of dormant seeds by consuming

litter containing allelopathic compounds (Jameson 1970;

Schott and Pieper 1987), and altering the nutrient, water,

microbial, temperature, and light regimes of the seedbed

(Koniak 1985; Blank and others 1995). Chemical factors in

wood smoke or burned soil have been found to promote

germination of certain species, including coyote tobacco

(Baldwin and others 1994) and Indian ricegrass (Blank and

Young 1998).

Three-Year Community Dynamics

For some species, frequency remained roughly constant

across years, while for other species, frequency changed in

the burned and/or unburned plots (table 2). Slight changes

may represent error due to species being overlooked or

misidentified, or sampling at different periods of phenological development in different years. For the majority of
USDA Forest Service Proceedings RMRS-P-21. 2001 181

Plant Community Dynamics of Burned and Unburned Sagebrush and Pinyon-Juniper Vegetation in West-Central Utah Ott, McArthur, and Sanderson

Table 2—Frequency (number of plots in which species were present) by treatment and year for vascular plant species recorded at four sites in westcentral Utah following 1996 wildfires. Values without parentheses are for 100 m2 plots; values in parentheses are for 1 m2 subplots, shown

if greater than zero. Maximum frequency per treatment/year combination is 16.

Unburned Burned

Species name Common name Sitesa 1997 1998 1999 1997 1998 1999

Native shrubs and trees

Artemisia tridentata Big sagebrush C G J T 12 (7) 12 (5) 12 (7) 1 1 1

Chrysothamnus nauseosus Rubber rabbitbrush ——J— 000111

Chrysothamnus viscidiflorus Viscid rabbitbrush ——J T 8 (5) 8 (4) 8 (5) 0 0 0

Cercocarpus montanus Mountain mahogany C——— 111111

Ephedra nevadensis Nevada ephedra ——J T 555111

Eriogonum corymbosum Fremont’s buckwheat C——— 111000

Eriogonum ovalifolium Cushion buckwheat ———T 232000

Gutierrezia sarothrae Broom snakeweed C G J T 555566

Juniperus osteosperma Utah juniper C G J T 15 (3) 15 (3) 15 (3) 1 1 1

Leptodactylon pungens Prickly phlox C G—— 1 (1) 1 (1) 1 (1) 1 1 0

Opuntia polyacantha Pricklypear C—J T 555111

Pediocactus simpsonii Simpson’s footcactus ———T 100000

Pinus edulis Colorado pinyon pine C——— 344000

Purshia mexicana Cliffrose ——J— 111000

Purshia tridentata Bitterbrush C G—— 4 (1) 4 (1) 4 (1) 0 0 0

Quercus gambelii Gambel oak C——— 121222

Symphoricarpos oreophilus Mountain snowberry C——— 100000

Tetradymia canescens Gray horsebrush ——J— 222000

Native grasses

Elymus elymoides Bottlebrush squirreltail C G J T 16 (12) 16 (11) 16 (9) 14 (3) 13 (3) 13 (3)

Elymus smithii Western wheatgrass —G—T 000322

Elymus spicatus Bluebunch wheatgrass C G—T 8 (5) 8 (4) 8 (4) 6 (1) 6 6 (1)

Festuca octoflora Sixweeks fescue ——J— 110000

Koeleria macrantha Prairie junegrass C——— 4 3 (2) 4 (2) 2 3 3

Poa fendleriana Muttongrass C G J T 7 (4) 12 (4) 7 (4) 6 (1) 6 (1) 3

Poa secunda Sandberg bluegrass C——T 5 (2) 4 (2) 2 (2) 4 (2) 4 2 (1)

Stipa comata Needle-and-thread — J— 000111

Stipa hymenoides Indian ricegrass C G J T 11 (1) 11 (1) 10 (1) 8 (1) 8 (1) 8 (1)

Exotic grasses

Bromus japonicus Japanese brome C——T 1 1 (1) 0340

Bromus tectorum Cheatgrass C G J T 16 (15) 16 (16) 16 (16) 16 (13) 16 (16) 16 (16)

Hordeum jubatum Foxtail barley C——— 000110

Secale cereale Cultivated rye ——J— 010000

Setaria viridis Green bristlegrass C——— 000100

Seeded grasses

Agropyron cristatum Crested wheatgrass C G J— 2 1 2 5 (3) 6 (4) 7 (5)

Bromus inermis Smooth brome C—J— 0 0 0 4 (4) 5 (4) 5 (4)

Dactylis glomerata Orchardgrass C——— 000010

Elymus elongatus/hispidus Tall/Intermediate C G J— 0 0 0 4 (1) 7 (1) 10 (1)

wheatgrass

Elymus junceus Russian wildrye C G—— 0 0 0 0 5 (2) 5 (2)

Seeded shrubs and forbs

Atriplex canescens Fourwing saltbush —G—— 000100

Medicago sativa Alfalfa C——— 0 0 0 4 (1) 4 (2) 1 (1)

Melilotus officinalis Yellow sweetclover C——— 0 0 0 4 (1) 4 0

Sanguisorba minor Small burnet C——— 0 0 0 4 (1) 4 (1) 3 (1)

Exotic forbs

Alyssum desertorum Desert alyssum C G J T 12 (9) 13 (11) 13 (12) 6 3 7 4 7 2

Camelina microcarpa Falseflax —G—— 1 3 (2) 3 (3) 3 4 (1) 3 (2)

Chenopodium album Lambsquarter C G J— 010210

Erodium cicutarium Storksbill ——J— 0 0 0 1 3 3 (1)

Lactuca serriola Prickly lettuce C G J T 0 6 (4) 5 (1) 12 11 (7) 12 (7)

Malcolmia africana African mustard —G J T 100630

Polygonum aviculare Knotweed C —— 000010

Ranunculus testiculatus Bur buttercup C G—T 8 (6) 8 (6) 7 (6) 8 (5) 4 4 (2)

Salsola iberica Russian thistle —G J— 0 1 (1) 0 0 0 1

Salsola paulsenii Barbwire Russian thistle ———T 000100

Sisymbrium altissimum Tumblemustard —G J T 1 6 (2) 7 (1) 2 9 (7) 11 (6)

Tragopogon dubious Yellow salsify C G J T 4 1 3 (1) 7 8 (2) 8 (5)

Native annual forbs

Camissonia boothii Booth’s camissonia ——J— 000100

Collinsia parviflora Blue-eyed Mary C——— 1 2 (1) 0 4 (1) 0 0

Collomia grandiflora Large collomia C——— 000200

(con.)
182 USDA Forest Service Proceedings RMRS-P-21. 2001

Ott, McArthur, and Sanderson Plant Community Dynamics of Burned and Unburned Sagebrush and Pinyon-Juniper Vegetation in West-Central Utah

Cryptantha ambigua Wilke’s cryptanth C——— 000100

Cryptantha cineria James’ cryptanth —G—— 1 (1) 1 (1) 0000

Cryptantha micrantha Dye cryptanth ——J— 010000

Cryptantha nevadensis Nevada cryptanth C G — 100320

Cryptantha (unidentified) Cryptanth C—J T 0 1 3 (1) 2 1 2

Descurainia pinnata Pinnate tansymustard C G J T 3 (1) 4 (3) 2 (1) 12 (3) 16 (2) 3

Draba verna Spring draba —G—— 000100

Epilobium brachycarpum Autumn willowherb C——T 0 1 0 2 (1) 2 4 (1)

Eriogonum deflexum Skeleton buckwheat —G J— 5 (1) 1 0 5 (2) 3 (1) 1

Eriogonum palmeranum Palmer’s buckwheat —G—— 000100

Galium aparine Common bedstraw C——— 000200

Gayophytum decipiens Deceptive groundsmoke ——J— 100000

Gayophytum lasiospermum Hairyseed groundsmoke C G—T 0 0 0 8 (1) 0 0

Gilia giliodes Collomia gilia C——T 0 0 0 5 (4) 0 0

Gilia inconspicua Floccose gilia C G J T 4 6 (1) 5 (2) 15 (8) 4 (1) 5

Gilia polycladon Spreading gilia ——J— 000200

Helianthus annuus Common sunflower C——— 000100

Lappula occidentalis Western stickseed C—J— 100110

Mentzelia albicaulis Whitestem blazingstar C G J T 0 0 0 8 (3) 1 0

Microsteris gracilis Little polecat C——— 4 (3) 4 (3) 3 (3) 3 0 0

Mimulus rubellus Monkey-flower C——— 000200

Nicotiana attenuata Coyote tobacco C G—T 0 0 0 7 (1) 2 0

Phacelia ivesiana Ives’ Phacelia —G—— 000200

Polygonum douglasii Douglas’ knotweed C——— 3 (1) 4 (1) 3 (1) 4 2 3

Solanum triflorum Cutleaf nightshade C——— 000200

Verbena bracteata Prostrate verbena C—J— 000222

Native perennial forbs

Agoseris glauca Mountain dandelion C——T 2 (1) 3 0 4 2 2 (1)

Allium acuminatum Acuminate wild onion C——T 0 0 0 2 1 (1) 0

Antennaria dimorpha Low pussytoes C——— 020000

Arabis drummondii Drummond’s rockcress ———T 120200

Arabis holboellii Holboell’s rockcress C G J T 8 (1) 7 (1) 3330

Argemone munita Prickly-poppy C G—— 000553

Astragalus calycosus Torrey’s milkvetch —G J T 9 (1) 9 (1) 8 (2) 4 (2) 3 (1) 2

Astragalus convallarius Rush milkvetch —G—— 1 (1) 1 (1) 1 (1) 1 0 1

Astragalus eurekensis Eureka milkvetch —G J— 112001

Astragalus lentiginosus Freckled milkvetch —G J— 344553

Astragalus piutensis Sevier milkvetch C——T 4 (1) 4 (1) 2310

Astragalus utahensis Utah milkvetch C——T 2 (1) 41200

Astragalus (unidentified) Milkvetch ———T 000001

Calochortus nuttallii Sego lily C G—T 7 (2) 4 (1) 3 (1) 7 3 3

Castilleja chromosa Common paintbrush ——J— 111000

Chaenactis douglasii Douglas’ dustymaiden C G J T 10 (2) 11 (2) 10 (2) 9 (2) 8 (1) 2 (1)

Chaetopappa ericoides Rose-heath ———T 2 (1) 2 (1) 2 (1) 0 0 0

Cirsium wheeleri Wheeler’s thistle C——— 010122

Comandra umbellata Bastard toadflax ———T 2 (1) 1 (1) 1 (1) 2 1 2

Crepis occidentalis Western hawksbeard C——T 4 0 0 4 (1) 4 (1) 4 (2)

Cryptantha humilis Dwarf cryptanth —G—T 5 3 (1) 5 (2) 1 1 1

Erigeron aphanactis Hairy daisy C——T 120323

Erigeron engelmanii Engelmann’s daisy —G J— 001001

Linum perenne Blue flax —G—T 2 2 2 (1) 1 1 1

Lygodesmia grandiflora Showy rushpink ——J— 221000

Machaeranthera canescens Hoary aster —G—T 5 (1) 5 (1) 5 (2) 3 3 2

Oenothera caespitosa Tufted evening primrose ——J— 1 1 (1) 2 (1) 0 0 0

Orobanche multiflora Cancerroot ——J T 141000

Petradoria pumila Rock goldenrod C——T 3 (1) 2 (1) 2 (1) 0 0 0

Phlox austromontana Desert phlox C G—T 8 (5) 6 (6) 8 (6) 2 2 2

Phlox longifolia Longleaf phlox C G J T 11 (5) 9 (2) 7 (4) 10 (2) 3 (1) 3 (1)

Physaria chambersii Chamber’s twinpod ———T 000110

Senecio multilobatus Uinta groundsel C G J T 7 (1) 9 (2) 6 (2) 2 3 (1) 0

Sphaeralcea coccinea Common globemallow —G—— 3 (1) 2 (1) 3 (1) 3 3 3 (1)

Sphaeralcea grossulariifolia Gooseberry globemallow ——J T 2 2 2 4 (1) 3 (1) 5

Stanleya pinnata Prince’s plume ——J— 111000

Streptanthus cordatus Twistflower —G J— 4 (2) 4 (2) 4 (2) 3 2 (1) 0

Vicia americana American vetch —G—— 3 (2) 3 (2) 3 (2) 4 (2) 4 (2) 2

Viola spp. Violet ———T 010000

Zigadenus paniculatus Foothills death camas C G—T 3 (1) 2 2 (1) 1 0 0

a

Study sites where species was recorded; C = Cunningham, G = Gilson, J = Jericho, T = Twin.

Table 2—Cont.

Unburned Burned

Species name Common name Sitesa 1997 1998 1999 1997 1998 1999
USDA Forest Service Proceedings RMRS-P-21. 2001 183

Plant Community Dynamics of Burned and Unburned Sagebrush and Pinyon-Juniper Vegetation in West-Central Utah Ott, McArthur, and Sanderson

Table 3—Species with greatest difference in frequency and cover between burned and unburned treatments across

four sites in west–central Utah following 1996 wildfires. Based on 1997 data from 100 m2 size plots. Earlyseral species have low value for frequency index (unburned frequency minus burned frequency) and cover

index (mean unburned cover minus mean burned cover); late–seral species have high values for these

indices. Seeded species are omitted.

Frequency Cover

index index

Early-seral Early-seral

Lactuca serriola (EAF) –15 Bromus tectorum (EAG) –7.3

Descurainia pinnata (NAF) –12 Gilia inconspicua (NAF) –3.3

Gilia inconspicua (NAF) –11 Nicotiana attenuata (NAF) –1.3

Gayophytum lasiospermum (NAF) –8 Descurainia pinnata (NAF) –1.2

Mentzelia albicaulis (NAF) –8 Lactuca serriola (EAF) –0.8

Nicotiana attenuata (NAF) –8 Alyssum desertorum (EAF) –0.7

Argemone munita (NPF) –5 Ranunculus testiculatus (EAF) –0.7

Malcolmia africana (EAF) –5 Crepis occidentalis (NPF) –0.5

Sisymbrium altissimum (EAF) –4 Mentzelia albicaulis (NAF) –0.4

Tragopogon dubius (EAF) –4 Sisymbrium altissimum (EAF) –0.4

Late-seral Late-seral

Alyssum desertorum (EAF) 4 Arabis holboellii (NPF) 0.2

Astragalus calycosus (NPF) 4 Gutierrezia sarothrae (NS) 0.2

Ephedra nevadensis (NS) 4 Petradoria pumila (NPF) 0.3

Opuntia polyacantha (NS) 4 Oryzopsis hymenoides (NPG) 0.4

Purshia tridentata (NS) 4 Poa fendleriana (NPG) 0.4

Arabis holboellii (NPF) 5 Phlox austromontana (NPF) 2.7

Phlox austromontana (NPF) 6 Sitanion hystrix (NPG) 3.8

Chrysothamnus viscidiflorus (NS) 8 Chrysothamnus viscidiflorus (NS) 4.5

Artemisia tridentata (NS) 10 Artemisia tridentata (NS) 13.8

Juniperus osteosperma (NT) 15 Juniperus osteosperma (NT) 17.0

Key to abbreviations: Origin: E = exotic, N = native; Longevity: A = annual, P = perennial; Form: F = forb, G = grass, S = shrub,

T = tree.

species encountered, cover and density were low and followed approximately the same trends as frequency. Widespread species (or genera) having high mean cover or density

are shown in tables 4 and 5. Note that the means in these

tables are based on only three sites (Jericho, Gilson, and

Twin) where burned treatments had not been aerially seeded.

Some seeded species were found in plots at the Jericho and

Gilson sites, probably because of drift from nearby aerial

seedings. However, cover of these seeded species was low

(less than 1 percent) and their contribution to community

dynamics was minimal.

In general, fewer changes were observed in the unburned

treatment than the burned treatment, as would be expected

because of the slower rate of successional change in late seral

stages (Austin 1987). Frequency, density, and cover remained relatively stable for most perennial species in the

unburned treatment, although some perennial forbs, such

as Holboell’s rockcress, sego lily, and longleaf phlox, showed

a trend of decreasing frequency over time (table 2). Some

annuals, such as the exotic forbs tumblemustard and falseflax

(Camelina microcarpa), increased in frequency and density

over time in the unburned treatments (tables 2, 5). Certain

other annual and short-lived perennial species (such as,

floccose gilia, Douglas’ dustymaiden, Uinta groundsel (Senecio multilobatus), prickly lettuce, and desert alyssum) had

slightly higher frequency, density, and/or cover in 1998 in

the unburned treatment than in other years (tables 2, 4, 5).

These fluctuations of short-lived species in the unburned,

late-seral vegetation are likely related to climatic fluctuations, such as the observed higher precipitation during the

winter and spring of 1998 (NOAA 1998; fig. 2). Another

potential factor is increased dispersal from the nearby burned

areas. Prickly lettuce was absent from the unburned plots in

1997, but present in six unburned plots in 1998, possibly as

a result of seed dispersal from the 1997 crop of this species

in the burned areas.

In the burned treatment, most species of native grasses,

shrubs, and trees changed little in frequency, density, and

cover between years. Muttongrass (Poa fendleriana) and

Sandberg bluegrass (Poa secunda) fluctuated in frequency

(table 2), but these species are easy to overlook when dormant and may have sometimes been missed at some plots.

Some exotic species (such as, cheatgrass, tumblemustard,

falseflax, and prickly lettuce) showed an increasing trend

over time in the burned treatment, while other exotic species

(such as, Japanese brome (Bromus japonicus), bur buttercup (Ranunculus testiculatus), desert alyssum, and African

mustard) showed declining trends (tables 2, 4, 5). On the

other hand, most native forbs decreased over time, with

exceptions such as Crepis occidentalis, Erigeron aphanactis,

Epilobium brachycarpum, Machaeranthera canescens, Phlox

austromontana, Sphaeralcea coccinea, S. grossulariifolia,

and Verbena bracteata, which remained stable or increased

in frequency, density, and/or cover over time in the burned

treatment (tables 2, 4, 5).
184 USDA Forest Service Proceedings RMRS-P-21. 2001

Ott, McArthur, and Sanderson Plant Community Dynamics of Burned and Unburned Sagebrush and Pinyon-Juniper Vegetation in West-Central Utah

Table 4—Mean percent cover of synthetic species groups and selected species or genera, in burned and unburned treatments across 3 years, averaged

across three sites in west-central Utah. Values without parentheses are for 100 m2 plots; values in parentheses are for 1 m2 subplots. Letters

following species group means show statistical significance according to a mixed model, first order autoregressive analysis with mean

separation by the Tukey adjustment. Across rows, means with the same letter were not significantly different at alpha = 0.05.

Unburned Burned

Species 1997 1998 1999 1997 1998 1999

Native shrubs and trees 40.6a (11.5) 33.9a (14.5) 33.7a (14.3) 0.4b (0) 0.5b (0) 0.7b (0)

Artemisia tridentata 18.1 (7.9) 14.4 (11.5) 14.2 (10.6) + (0) + (0) + (0)

Chrysothamnus viscidiflorus 6.0 (3.5) 4.9 (3.0) 4.9 (3.6) 0 (0) 0 (0) 0 (0)

Juniperus osteosperma 15.7 (+) 13.8 (+) 13.8 (+) + (0) + (0) + (0)

Native grasses 8.5a (8.2e) 9.6a (9.4e) 6.3a (9.3e) 3.2a (1.0e) 4.4a (3.2e) 4.1a (1.5e)

Elymus elymoides 5.9 (6.5) 5.5 (6.8) 4.5 (6.9) 1.1 (0.2) 1.3 (1.0) 1.1 (1.0)

Elymus smithii 0 (0) 0 (0) 0 (0) 0.5 (0) 0.5 (0) 1.5 (0)

Elymus spicatus 0.6 (0.3) 0.8 (0) 0.6 (0) 0.8 (0.1) 0.8 (0) 0.8 (+)

Poa spp. 1.2 (1.4) 2.7 (2.6) 0.9 (2.3) 0.5 (0.5) 1.5 (2.1) 0.1 (+)

Stipa hymenoides 0.8 (+) 0.6 (+) 0.4 (0.2) 0.3 (0.1) 0.3 (0.1) 0.5 (0.3)

Exotic grasses* 19.0b (9.7f) 22.0bc (16.8f) 17.0b (9.1f) 28.6bd (28.0fg) 69.8a (75.7e) 54.7acd (54.6eg)

Exotic forbs 1.8a (2.4e

) 1.3a (2.8e) 1.6a (1.8e) 4.4a (3.6e) 7.8a (11.0e) 8.5a (5.4e)

Alyssum desertorum 0.3 (0.4) 0.4 (1.5) 0.6 (1.2) 0.7 (0.6) 0.2 (0.5) 0.2 (+)

Lactuca serriola 0 (0) 0.2 (0.2) 0.2 (+) 0.8 (0) 0.8 (0.4) 1.3 (2.3)

Sisymbrium altissimum + (0) 0.3 (0.8) 0.3 (+) 0.3 (0) 5.6 (9.7) 4.8 (2.1)

Native annual forbs 0.5ab (0.2f) 0.5ab (0.3ef) 0.3b (0.1f) 8.3a (8.2e) 1.3ab (0.5f) 0.4b (+f)

Gilia spp. 0.2 (0) 0.3 (+) 0.2 (0.1) 3.7 (3.9) 0.1 (0.3) 0.2 (0)

Mentzelia albicaulis 0 (0) 0 (0) 0 (0) 0.5 (1.3) 0 (0) 0 (0)

Nicotiana attenuata 0 (0) 0 (0) 0 (0) 1.7 (1.3) 0.1 (0) 0 (0)

Native perennial forbs 8.1a (5.6e) 9.5a (6.3e) 8.5a (7.5e) 5.0a (3.8e) 3.8a (2.4e) 2.1a (0.6e)

Astragalus spp. 0.9 (0.3) 1.0 (0.6) 0.6 (0.3) 0.9 (0.1) 0.8 (0.3) 0.3 (0)

Phlox austromontana 3.1 (2.3) 4.1 (1.8) 4.2 (2.6) + (0) + (0) + (0)

Sphaeralcea spp. 0.4 (0.1) 0.4 (+) 0.4 (0.1) 0.9 (0.2) 0.5 (+) 0.6 (0.1)

Vicia americana 0.6 (0.5) 0.5 (1.5) 0.3 (1.4) 0.4 (0.8) 0.6 (1.5) 0.1 (0)

*Exotic grass mean cover is equivalent to mean cover of Bromus tectorum

Table 5—Mean density per m2 of selected species, based on counts in 1 m2 plots, in burned and unburned

treatments across 3 years, averaged across three sites in west-central Utah.

Unburned Burned

Species 1997 1998 1999 1997 1998 1999

Native grasses

Elymus elymoides 9.1 8.8 7.2 0.2 0.6 0.3

Elymus spicatus 0.4 0 0 0.1 0 0.2

Poa fendleriana 1.4 2.6 7.5 2.5 0.7 0

Stipa hymenoides 0 0 0.2 0.1 0.1 0.1

Bromus tectorum 84.1 76.3 89.2 55.3 157.5 345.8

Exotic forbs

Alyssum desertorum 14.8 27.3 19.8 3.0 10.3 0.4

Camelina microcarpa 0 0.2 2.1 0 0.3 2.3

Lactuca serriola 0 1.4 0.3 0 1.5 26.8

Ranunculus testiculatus ? ? 9.0 62.3 0 1.0

Sisymbrium altissimum 0 0.5 0.6 0 5.2 6.2

Native annual forbs

Gilia inconspicua 0 0.2 0.3 3.6 0.4 0

Mentzelia albicaulis 0 0 0 3.5 0 0

Native perennial forbs

Astragalus calycosus 0.3 0.3 0.2 0.3 0.1 0

Phlox austromontana 3.8 2.3 3.7 0 0 0

Sphaeralcea coccinea 0.3 0.3 0.3 0 0 0.2

Sphaeralcea grossulariifolia 0 0 0 0.6 0.1 0

Vicia americana 3.8 2.8 2.9 2.6 4.5 0
USDA Forest Service Proceedings RMRS-P-21. 2001 185

Plant Community Dynamics of Burned and Unburned Sagebrush and Pinyon-Juniper Vegetation in West-Central Utah Ott, McArthur, and Sanderson

Results of mixed model analysis of synthetic cover for

species groups are shown in table 4. Although, in the burned

treatment, synthetic cover of native perennial forbs had a

decreasing trend over time, and synthetic cover of exotic

forbs had an increasing trend over time, these trends were

not statistically significant. The decrease in native annual

forb cover between 1997 and 1999 in the burned treatment

appeared statistically significant, although the native annual forb group did not meet the assumption of normality

according to the Shapiro-Wilk statistic. Only the native

shrub and tree, exotic grass, and native perennial forb

groups clearly met the assumption of normality for this

model. Native shrubs and trees had significantly greater

cover in the unburned treatment than the burned treatment

for all years.

The most notable trend observed was a more than two-fold

increase in exotic grass cover in the burned areas between

1997 (ca. 28 percent) and 1998 (ca. 70 percent in large plots

and 76 percent in small plots). The trend was statistically

significant (table 4). Cheatgrass density likewise increased

between 1997 (55 per m2

) and 1998 (157 per m2), and

continued to increase to 345 per m2 in 1999 (table 5). These

data indicate that cheatgrass, the principal exotic grass, had

an explosive population increase in the early-seral environment. Other authors have reported similar responses for

this species following fire (Young and Evans 1978; Hosten

and West 1994).

The decline of certain species over time in the burned

treatment, concurrent with the increase of cheatgrass and

other exotic species, suggests that competition may have

Precipitation

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Figure 2—Monthly precipitation from August 1996 to August 1999 at three weather

stations in west-central Utah (source: National Oceanic and Atmospheric Survey).
186 USDA Forest Service Proceedings RMRS-P-21. 2001

Ott, McArthur, and Sanderson Plant Community Dynamics of Burned and Unburned Sagebrush and Pinyon-Juniper Vegetation in West-Central Utah

shaped the observed dynamics. Factors such as climatic

events and soil changes brought about by the fire may have

interacted with competition to cause some populations to

increase and others to decline. High precipitation during the

cool season of the 1997 to 1998 period (fig. 2) undoubtedly

contributed to the explosive increase of cheatgrass.

Cheatgrass then appeared to displace or subdue many

native forbs, which otherwise might have increased and

reached peaks of cover during the second to fifth growing

season following the fires (Everett and Ward 1984). Forb

declines could also be related to periods of low precipitation,

such as late summer of 1998 (fig. 2).

Comparison of Tree Canopy and

Interspace

The successional dynamics described above did not proceed uniformly in all portions of the burned areas. Dynamics

occurred at different rates in interspace and subcanopy

areas. Although we did not detect delayed invasion of

cheatgrass into the haloes of burned shrubs, as reported by

Young and Evans (1978), we did observe a delay under the

skeletons of juniper trees. Figure 3 illustrates this observation through a depiction of the spatial relationship between

cheatgrass basal cover and tree canopy along the 1998

burned and unburned step-point transects at the Gilson

study site. Along the unburned transects, cheatgrass was

relatively rare, and was found most frequently beneath the

canopy of living trees. This pattern may have been the result

of more favorable nutrient, water, or seedbed characteristics

in the subcanopy litter zone. The pattern also suggests that

cheatgrass was resistant to allelopathic compounds in the

juniper litter at that site. Along the burned transects,

Unburned Transect

Burned Transect

Juniper (live canopy cover) Cheatgrass (basal cover)

Juniper (dead canopy cover) Cheatgrass (basal cover)

Figure 3—Spatial relationship between cheatgrass and juniper canopy along

step-point transects in burned and unburned treatments of the Gilson study site

in 1998 (second year post-fire). For each treatment, a composite of four

transects of 40 points each, at intervals of 1 m is shown.

cheatgrass cover was much greater, but was concentrated in

the interspaces rather than beneath the dead trees, even

after two seasons of population increase.

As noted previously, heat loads appeared to have been

high beneath most burned trees at our study sites. Plants,

seeds, and litter were consumed beneath the trees, and

hydrophobic soil conditions may have been generated (Blank

and others 1995). Cheatgrass, which germinates best on

surfaces with litter or microtopographic relief (Young and

others 1976), did not immediately recolonize areas beneath

burned trees. Factors inhibiting the establishment of

cheatgrass in the subcanopy zones of dead junipers began to

break down by the second year following the fire, when rings

of newly established cheatgrass were frequently observed

around the edges of burned juniper canopies. To the inside

of these cheatgrass rings, we typically observed a ring of

exotic annual forbs, dominated by mustards (family

Cruciferae) such as tumblemustard, desert alyssum, and

falseflax. Both the mustard and cheatgrass fronts had moved

concentrically inward by the third season following the fire.

The foregoing successional pattern is illustrated for a 1 m2

plot in the subcanopy zone of a dead juniper at the Gilson site

(fig. 4). Density and cover data for this plot are shown in

table 6, along with data for another meter-square plot that

was located in an interspace zone. The plot in the subcanopy

zone (fig. 4; table 6a) consisted primarily of bare soil and two

species of native annual forbs (coyote tobacco and floccose

gilia) in 1997. These species were replaced in 1998 by exotic

species, primarily tumblemustard. By 1999, cheatgrass was

the dominant species in the subcanopy plot, with cover of 85

percent. Even though cheatgrass invasion was delayed by a

year in the subcanopy plot compared to the interspace plot

(table 6b), density of this aggressive, exotic grass was approximately 400 per m2 in both plots by 1999. In the interspace
USDA Forest Service Proceedings RMRS-P-21. 2001 187

Plant Community Dynamics of Burned and Unburned Sagebrush and Pinyon-Juniper Vegetation in West-Central Utah Ott, McArthur, and Sanderson

Figure 4—Photographic record of a 1 m2 plot

at the Gilson burned area, showing a representative sequence of changes occurring in

the subcanopy zone of a burned juniper tree:

(a) 1997 (first year after fire) bare ground/

native annual forbs; (b) 1998 (second year

after fire) tumblemustard dominant; (c) 1999

(third year after fire) cheatgrass dominant.

Also see table 6.

a

b

c
188 USDA Forest Service Proceedings RMRS-P-21. 2001

Ott, McArthur, and Sanderson Plant Community Dynamics of Burned and Unburned Sagebrush and Pinyon-Juniper Vegetation in West-Central Utah

Table 6—Three-year post-fire trends of cover and density count by species for two representative 1 m2 plots of the

Gilson study site burned treatment.

1997 1998 1999

Percent Percent Percent

Species/category Count cover Count cover Count cover

Tree canopy plot (see also fig. 2)

Bromus tectorum 0 0 20 10 ~400 85

Camelina microcarpa 0 0 0 0 25 5

Descurainia spp. 002200

Gilia inconspicua 120000

Lactuca serriola 0 0 1 <1 4 <1

Nicotiana attenuata 1 15 0000

Sisymbrium altissimum 0 0 18 70 4 <1

Tragopogon dubius 000011

Exposed litter — 1 — 15 — 10

Exposed rock — 14 — 10 — <1

Exposed bare soil — 70 — 45 — <1

Tree interspace plot

Alyssum desertorum 29 5 ~100 5 0 0

Bromus tectorum ~150 30 ~400 98 ~400 65

Eriogonum deflexum 10 50000

Gilia inconspicua 12 80000

Lactuca serriola 000061

Mentzelia albicaulis 40 15 0000

Ranunculus testiculatus 40 10 0000

Sisymbrium altissimum 0 0 4 1 1 <1

Vicia americana 10 5 22 800

Exposed litter — 15 — 1 — 35

Exposed rock — 10 — <1 — 0

Exposed bare soil — 5 — <1 — <1

plot, the 1998 cheatgrass crop contributed to the 1999 litter

cover, with the result that cheatgrass litter and new

cheatgrass growth together occupied nearly 100 percent of

the plot surface in 1999. The decline of species such as

American vetch (Vicia americana) in the interspace plot may

have been related to the expansion of cheatgrass and/or drier

conditions in 1998 and 1999.

Comparison of Study Sites

While some patterns and trends were common to all study

sites, the uniqueness of each site was also evident. Steppoint transect results illustrate some of the differences in

composition and cover between sites in 1998 (table 7). One of

the categories with the highest variability between sites was

tree canopy cover, which was highest at Cunningham and

lowest at Twin. Cunningham also had several woody species

not recorded elsewhere (table 2), including pinyon (Pinus

edulis), gambel oak (Quercus gambelii), mountain mahogany

(Cercocarpus montanus), and mountain snowberry

(Symphoricarpos oreophilus). Compared to the other study

sites, Cunningham has higher elevation, steeper slopes, and

rockier substrate (table 1). These characteristics indicate

that Cunningham is probably a “true” pinyon-juniper site,

whereas the other sites are probably sagebrush or sagebrush

steppe that have been more recently invaded, to different

degrees, by juniper.

The unburned communities at all sites had greater cover

of exotic annual grass than native perennial grass (table 7).

Prolonged grazing of livestock has probably occurred at

these sites and contributed to the observed pattern. Of the

unburned treatments, Cunningham had the lowest basal

cover of native grass (2 percent) relative to exotic grass (12

percent) in the 1998 step-point results (table 7). The disparity between native grass and exotic grass cover was even

greater in the Cunningham burned treatment (2 percent

native, 22 percent exotic), but not as high as the burned

treatments of other sites, where exotic grass cover ranged

from 45 to 60 percent (table 7). The lower exotic grass cover

at Cunningham appears to have been directly related to the

presence of seeded species, particularly seeded grasses,

which had 17 percent cover in 1998 (table 7). Crested

wheatgrass (Agropyron cristatum), intermediate wheatgrass

(Elymus hispidus), and smooth brome (Bromus inermis), the

primary seeded grasses at the Cunningham site, have been

shown to be good cheatgrass competitors (Francis and Pyke

1996; Wicks 1997; Whitson and Koch 1998). To a lesser

degree, native perennial grasses such as bluebunch wheatgrass and bottlebrush squirreltail are also competitive with

cheatgrass (Reichenberger and Pyke 1990; Stevens 1997).

Evidence suggests that cheatgrass proliferation following

fire can be suppressed by a good cover of native perennial

grasses (West and Hassan 1985). These findings highlight

the importance of perennial grasses for rehabilitation or

restoration of cheatgrass-infested areas.
USDA Forest Service Proceedings RMRS-P-21. 2001 189

Plant Community Dynamics of Burned and Unburned Sagebrush and Pinyon-Juniper Vegetation in West-Central Utah Ott, McArthur, and Sanderson

Conclusion_____________________

The study presented here offers a rough glimpse of fire

effects and successional characteristics of numerous species

occurring in the sagebrush and pinyon-juniper communities

of west-central Utah. We found many native species in lateseral sagebrush and pinyon-juniper communities at our

study sites, even though these sites had been disturbed by

prolonged livestock grazing and the introduction of exotic

species. Fire in these communities resulted in a shift in

dominance from woody to herbaceous species, especially

annual species. The post-fire community continued to change

over the 3-year period of observation. Certain species increased while others declined or remained relatively stable.

Exotic species, particularly cheatgrass, appear to have

strongly influenced the character and rate of succession

observed. Beneath burned juniper trees, exotic annual mustards displaced native annual forbs, and may have created

conditions leading to their own displacement by cheatgrass.

Although exotic species undoubtedly had an impact, not all

exotic species were aggressive intruders, and not all native

species appeared to be adversely affected by the presence of

exotics.

An understanding of the dynamics and interactions among

the species that currently occupy these communities is

important for effective management and restoration efforts.

Complete restoration of degraded sagebrush and pinyonjuniper communities will be difficult because of the presence

of exotic species. Nevertheless, communities in which exotic

species are subordinate to competitive or tolerant native

species can perhaps be attained through restoration efforts.

The period immediately following fire is a window of opportunity in which intervention could favor native species.

Failure to seed burned sites will usually permit exotic

annuals to proliferate. The result may be stable systems

dominated by exotic annuals and a short fire-return cycle.

Acknowledgments ______________

This study was funded by the Utah State Office of the

Bureau of Land Management. We appreciate the support

and assistance given by BLM personnel, namely Pat Fosse,

Harvey Gates, and Don Proctor. We also wish to thank Lans

Stavast and Alex Parent for their field assistance, and we

thank Stan Kitchen and Kimball Harper for their helpful

review of this manuscript.

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Wicks, G. A. 1997. Survival of downy brome (Bromus tectorum) seed

in four environments. Weed Science 45:225–228.

Wright, H. A.; Neuenschwander, L F.; Britton, C. M. 1979. The role

and use of fire in sagebrush-grass and pinyon-juniper plant

communities: a state of the art review. Gen. Tech. Rep. INT-58.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Research Station. 48 p.

Young, J. A.; Evans, R. A. 1978. Population dynamics after wildfires

in sagebrush grasslands. Journal of Range Management 31:

283–289.

Young, J. A.; Evans, R. A.; Weaver, R. A. 1976. Estimating potential

downy brome competition after wildfires. Journal of Range Management 29:322–325.

Zschaechner, G. A. 1985. Studying rangeland fire effects: a case

study in Nevada. In: Sanders, K.; Durham, J.; and others, eds.

Rangeland fire effects: a symposium; 1984 November 27–29;

Boise, ID. Boise, ID: U.S. Department of the Interior, Bureau of

Land Management, Idaho State Office: 66–84.
192 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Jason L. Vernon and James N. Davis are Wildlife Biologists, Utah Division

of Wildlife Resources, Great Basin Research Station, 540 N. Main Street,

Ephraim, UT 84627. Val Jo Anderson is Professor of Range Management,

Department of Botany and Range Science, Brigham University, Provo, UT

84606.

Abstract—Pinyon-juniper woodlands have dramatically increased

in both tree density and distribution over the last 150 years. This

change led to depleted native herbaceous understory in pinyonjuniper woodlands. One method to increase herbaceous understory

is to remove the trees and aerially seed. The objective of this study

was to determine how variations of seed mixes used in past revegetation projects have affected residual native species.

Native herbaceous understory diversity and abundance were

significantly greater in chained and seeded sites than in nonchained sites (p ≤ 0.02 and p ≤ 0.05 respectively), although diversity

and abundance were low in both. Native herbaceous understory

richness was similar between chained/seeded sites and non-chained

pinyon-juniper sites. Seeding rates and mixtures showed low correlation with post-treatment native species diversity and abundance.

The post treatment combined abundance of crested wheatgrass

[Agropyron cristatum (L.) Gaertner] and intermediate wheatgrass

[Elymus hispidus (Opiz.) Meld.] was negatively associated with

native herbaceous understory diversity after two-way chaining and

seeding with exotic species (r2

 = 0.76).

Future revegetation projects, on sites similar to those in central

and southern Utah, should include a more site-specific approach to

increasing native herbaceous understory diversity or abundance

than the broad approach previously used in the revegetation efforts

examined here. If increasing native species diversity or abundance

are objectives in future revegetation projects, inclusion of adapted

native species in conjunction with decreasing the proportion of

exotic species in seed mixtures may be required.

Introduction ____________________

Pinyon-juniper [Pinus edulis Engelm. and Juniperus

osteosperma (Torr.) Little] woodlands cover approximately

18 million hectares throughout the Intermountain West

and approximately 6 million hectares in Utah (West 1984;

O’Brien and Woudenberg 1999). Over the last 150 years

pinyon-juniper woodlands have dramatically changed in

tree density (from an open savanna type with scattered trees

to a closed canopy community) and distribution (movement

of woodlands into lower and higher elevations) (Tausch

1999; West 1999).

Response of Residual Native Species After

Two-Way Chaining and Seeding in Utah

Jason L. Vernon

Val Jo Anderson

James N. Davis

The principal factors believed to contribute to the changes

in tree density and distribution of pinyon-juniper woodlands

include: (1) heavy livestock grazing following European

settlement (West 1984), (2) an increase in fire suppression

and corresponding decrease in fire frequency (West 1984;

Bunting 1994), (3) a change in climate with rising mean

annual temperatures (Ghil and Vautgard 1991), (4) cessation of the hunting, gathering and burning by populations of

indigenous people that occurred during the Little Ice Age

(Creque 1996; Tausch 1999), and (5) increasing atmospheric

CO2 levels that change community competitive interactions

in favor of dominance by large woody perennials (Polley and

others 1996; Farquhar 1997).

As pinyon-juniper woodlands become more dense and

spread into adjacent sagebrush-grass plant communities,

interspecific competition between trees and the understory

species increase. Pinyon and juniper trees influence understory plants in several ways: by shading, sub-canopy litter

accumulation and by the competition for soil moisture through

the development of an extensive and competitive shallow

root system (Schott and Pieper 1985). As mature trees obtain

dominance, the remaining understory species are severely

suppressed. Hurst (1975) and Dye and others (1995) report

that understory suppression generally varies inversely with

the tree overstory density. Additionally, Arnold and others

(1964) found that as canopy cover increases, basal cover of

grasses and forbs decrease.

Beginning in the early 1950s, earnest efforts were undertaken to improve the depleted pinyon-juniper ranges in the

Western United States through mechanical removal of the

pinyon-juniper overstory and replacement with a desirable

shrub-herbaceous understory. Early efforts focused on increasing forage for livestock, while later objectives were

expanded to include wildlife habitat restoration and watershed protection (Fairchild 1999; Roundy 1996). Early improvement techniques included: anchor chaining, cabling,

hula dozing, bulldozing, windrowing and burning, and chemical treatments. After extensive research, two-way anchor

chaining was most commonly employed because it was cost

efficient, effectively reduced pinyon-juniper tree densities

(Aro 1971; Parker 1971; Phillips 1977; Stevens 1999) and

prepared an excellent seedbed (Plummer and others 1968;

Stevens 1999). Two-way chaining entails dragging an anchor chain between two tractor crawlers one direction,

aerially seeding, and then back chaining in the opposite

direction to cover the seed and increase pinyon and juniper

tree mortality (Plummer and others 1968; Aro 1975; Stevens

and others 1975; Stevens 1999).

Due to understory suppression, pinyon-juniper woodlands

usually lack sufficient seed of grass, forb and browse species
USDA Forest Service Proceedings RMRS-P-21. 2001 193

Response of Residual Native Species After Two-Way Chaining and Seeding in Utah Vernon, Anderson, and Davis

for natural recovery of the community after treatment. To

establish desired vegetation cover, seeds of desired species

are often sown during treatment. Many successful revegetation projects in the Western United States resulted in

replacement of degraded plant communities with substitutes containing mostly exotic species.

Requirements for establishing native species from seed in

a rangeland setting were not fully understood in these early

revegetation efforts. Native species showed poor establishment, seed availability was low and the seed that was

available was relatively expensive (Pyke 1995). Additional

factors prohibiting native species from being included in

seed mixes were the inability of native plants to compete

with exotic weeds such as cheatgrass [Bromus tectorum L.]

and the susceptibility of native species to grazing (Anderson

and Marlette 1986; Roundy and Call 1988; Chambers and

Norton 1993). Extensive research was initiated on the establishment requirements of native plants, as well as several

species from Europe, Russia and Asia (Plummer and others

1968; Kilcher 1969; Monsen 1975). Through this research,

many exotic species demonstrated a better ability than

native species to successfully establish and persist under

arid conditions following chaining and seeding pinyonjuniper woodlands.

As a result of the success of selected exotic grasses, large

tracts of treated pinyon-juniper woodland were seeded;

generally with only a few exotic grass species dominating

seed mixtures. Species diversity following treatment was

not as much of a concern as the establishment of some type

of vegetation, whether native or exotic (Pyke 1995). Two

grasses in particular, crested wheatgrass [Agropyron

cristatumL.] and intermediate wheatgrass [Elymus hispidus

(Opiz) Meld], were used extensively for seeding rangelands

throughout the Western United States because they were

easily established and seed was readily available at low cost.

Additionally, with the aggressive habits of these grasses,

land managers felt they had found a tool to control weeds,

reduce soil erosion and maintain or increase grazing

capacities.

Plummer and others (1968) recognized several advantages for rangeland seedings to contain diverse seed mixtures rather than single species for several reasons. First,

many of the areas that are seeded have varying terrain,

micro-surface reliefs and climatic conditions. A diverse seed

mixture will allow adapted species to excel and persist in

different niches within the treated site. Second, a variety of

forage species can extend the season of use for both livestock

and wildlife. Third, a diverse community provides better

overall ground cover than single species stands. Fourth,

higher species diversity makes the community more resilient and shortens recovery time from long term disturbance.

Although the aforementioned recommendations were made

with respect to seed mixes in the late 1960s, few Federal land

managers prescribed diverse seed mixes in chaining treatments until the mid to late 1980s.

Pyke and Archer (1991) asserted that competitive relationships of species used in rangelands need to be identified

to determine if species can coexist and thereby facilitate

greater species diversity on the site. Furthermore, a diversity of species and growth forms would provide more stable

cover and more dependable productivity than a monoculture, because most sites are characterized by environmental

variability. Pyke (1995) points out that even though competitive exotic species may be effective in suppressing

weedy species, this same aggressive value may exclude

desirable native species as well. Compatibility and competitive relationships among plants in mixtures appear to be

rarely considered and research providing quantitative evidence is lacking.

Our objectives in this study were to determine whether

native species diversity, richness and abundance differ between two-way chained and seeded plots and adjacent nonchained pinyon-juniper woodlands in Utah. Secondly, are

there variables that can predict or explain these differences?

Methods _______________________

Study Sites

Ten sites were chosen for study throughout central and

southern Utah that represent typical pinyon-juniper

chainings. Study sites were located on state and Federal

lands where the treatments had been conducted by Bureau

of Land Management, U.S. Forest Service and/or Utah

Division of Wildlife Resources personnel. Seed mixtures

varied across sites with respect to seeding rate, number of

species/mix and the proportions of individual species within

each mix.

Chained sites ranged in age from 10 to 21 years since

treatment. Non-chained sites are best characterized as climax pinyon-juniper woodlands with high canopy cover and

sparse herbaceous understory. A few scattered shrubs were

present and dominant overstory species were pinyon pine

and Utah juniper. Chained sites contained mostly exotic

grasses with the majority of sites exhibiting some reencroachment of pinyon-juniper trees. Trees that were uprooted in the chaining treatment had been left on the ground

as litter. Plant composition on chained sites included some

native species that were present in the non-chained woodlands as well as exotic species that were seeded as part of

the two-way chaining and seeding treatments.

A pair of study plots were established at each site. One of

the paired plots was placed in pinyon-juniper woodland that

had been two-way chained and aerially seeded between

chaining passes with exotic grasses and forbs. The second

of the paired plots was placed in adjacent non-chained

pinyon-juniper woodland. To reduce any confounding effects

due to placement of study plots, specific criteria for elevation, aspect and slope were used. The range of acceptable

values for these variables were: (1) slopes below 20 percent,

(2) aspects of south or west exposure, and (3) elevations from

1,800 to 2,400 m.

Only native grass and forb species (hereafter referred to

as native herbaceous understory) were considered for native

diversity, richness and abundance. Native shrubs were

often included in seed mixtures, and inclusion of these

shrubs in data analysis would confound interpretations

about natural occurrences. Soil samples were collected at

each site and analyzed for physical and chemical properties

at Brigham Young University’s Soil and Plant Analysis

Laboratory. Although soil texture at the study sites varied,

the majority had soil texture characterized as sandy loam

or sandy clay loam.
194 USDA Forest Service Proceedings RMRS-P-21. 2001

Vernon, Anderson, and Davis Response of Residual Native Species After Two-Way Chaining and Seeding in Utah

Data Collection

Vegetation at each site was sampled along a 150 m

transect. A 1 m2 quadrat was placed on alternating sides of

the transect, beginning on the left at the zero meter mark,

and continuing at each 3 m interval for a total of 50 quadrats

per transect. Percent cover of vegetation and cryptogamic

crusts were estimated within each quadrat using a modified

Daubenmire cover class method (Daubenmire 1959; Bailey

and Poulton 1968). Nested frequency was determined for

each species and cover type following Smith and others

(1986, 1987). Nested frequency value were summed for each

species over all quadrats (50) to get a total value for the site

(a maximum value of 250).

Density of pinyon and juniper trees at 30 m intervals along

each transect sites was estimated using the point-centered

quarter method (Cottam and Curtis 1956). Canopy cover of

pinyon and juniper trees was measured along each transect

using the line-intercept method (Canfield 1941). Cover and

nested frequency data for non-vegetation variables were

also collected using the methods previously described. Nonvegetation variables include: litter, bare ground, rock and

pavement.

Species richness (S) was defined as the total number of

species encountered at a site. The Shannon-Weiner index

was used to determine species diversity (S ́) because it is

more sensitive to the abundance of rare species (Peet 1974).

S ́ is the number of species of equal abundance in a community and equates to the antilog of H ́ (∑(pi)(log2pi)), which is

often used as the index of species diversity when using the

Shannon-Weiner index (Krebs 1999).

Analysis

Differences in native herbaceous understory abundance,

richness and the percent change in diversity between treated

and native sites were tested using paired t-tests. The percent change in native species diversity was used so that

relative comparisons could be made across all sites. Additionally, differences in individual native species abundance

between chained and non-chained sites were also examined.

Regression analysis was used to develop predictive models for post-treatment changes in native species diversity

and abundance. In the models, percent change in native

species diversity and abundance between chained and nonchained woodlands were used as response variables. Time

since chaining is a continuum and was used as a predictor

variable to examine how time after treatment affects diversity and abundance across sites. Similarly, seeding rates are

a continuum and were used as predictor variables to examine the effect of different seeding rates on native species

diversity and abundance.

Several seed mix variables were examined including: total

lbs/acre of seed, total number of seeds/m2

, total number of

grass seeds/m2, the proportion of the seed mix that was

composed of crested and intermediate wheatgrasses seed

(both individually and combined) and the individual and

combined abundance of crested and intermediate wheatgrass after treatment.

Individual and combined abundance values for crested

and intermediate wheatgrasses after treatment, as measured by sum of nested frequency, were used as predictor

variables to examine possible post-treatment species effects.

Pure live seed (PLS) information was unavailable for most

sites. Therefore, data analysis concerning seed mixes was

estimated using bulk seed rate information obtained from

Range Development and Improvements (Vallentine 1989).

Results ________________________

Vegetation

Herbaceous understory cover was significantly greater

(p = <0.001) for the chained sites than for the non-chained

sites. Mean cover values were 18.9 percent and 1.9 percent

respectively. Native herbaceous cover was different (p =

0.192), with 1.9 percent cover on the non-chained sites and

4.6 percent cover on the chained sites. Seeded grasses were

not encountered on the non-chained sites.

Abundance, Diversity, and Richness

Native herbaceous understory abundance was significantly greater (p = 0.054) in the non-chained sites as compared to chained sites (fig. 1). Non-chained sites had 1.5

times greater sum of nested frequency values than chained

sites. Native herbaceous understory richness was similar

(p = 0.570) in the chained and non-chained sites averaging

11.4 species and 10.5 species respectively (fig. 2). Native

herbaceous understory Shannon-Weiner diversity values

were significantly greater (p = 0.022) in the non-chained

than in chained sites (fig. 3). Non-chained sites had mean

Shannon-Weiner diversity values nearly 2 times greater

than the chained sites. Differences in individual species

abundance were examined across all sites, however, individual native species were not encountered frequently enough

to allow for statistical analysis.

Figure 1—Native herbaceous understory species

abundance.

25.2

17.1

p=0.054

Native Species

0

5

10

15

20

25

30

Non-Chained Chained

Nested Frequency
USDA Forest Service Proceedings RMRS-P-21. 2001 195

Response of Residual Native Species After Two-Way Chaining and Seeding in Utah Vernon, Anderson, and Davis

Time Since Treatment

Regression analysis was completed for time since treatment with native herbaceous understory diversity and native

herbaceous understory abundance as response variables.

Low correlation between native herbaceous understory abundance or diversity and time since treatment indicated no

significant differences.

Seed Mixtures and Post-Treatment

Abundance

Regression analysis was completed for several seed mixture variables, the abundance of crested and intermediate

wheatgrasses after treatment as predictor variables with

native herbaceous understory abundance and diversity as

response variables (table 1). Native herbaceous understory

abundance was negatively associated with the proportion of

crested wheatgrass in the seed mix with an r2 value of 0.55.

Additionally, abundance of crested wheatgrass after treatment was negatively associated with native herbaceous

understory abundance with an r2

 value of 0.61.

All seed mix variables examined showed poor correlation

with native herbaceous understory diversity after treatment. However, the combined abundance of crested and

intermediate wheatgrass after treatment best predicted the

percent change in native herbaceous understory diversity

after treatment. The combined abundance is negatively

associated with an r2

 value of 0.76 (table 2).

Discussion _____________________

In this study, the non-chained sites had significantly

greater native herbaceous understory diversity and abundance than the chained area. Although analysis indicated

this was statistically significant, native herbaceous understory plants were rarely encountered and made up only a

small portion of the cover in both the chained and nonchained woodland. The response of native species after

two-way chaining and seeding pinyon-juniper sites can be

influenced by several factors. These include: (1) plant

density, condition and age of the plants left on the site

following treatment, (2) competition from any seeded species, (3) grazing by wildlife and livestock, and (4) climatic

conditions following treatment (Walker and others 1995).

These influences could effect native herbaceous understory

diversity and/or abundance after treatment.

Native species abundance, although significantly greater

in the non-chained sites, was considered very low across all

sites to begin with. Different factors can influence abundance of native species in both non-chained and chained

sites, but residual effects of the pinyon and juniper trees

may affect the native species in the chained area well after

the treatment was completed. The subsequent community

changes and the impact of competitive exotic species on

desirable and undesirable species after treatment with

crested and intermediate wheatgrass are generally well

known and can provide insight about the results of our

study.

Studies conducted by Heinrichs and Bolton (1950) in

Saskatchewan lead them to conclude that crested wheatgrass was a strong competitor and eventually excluded some

native species when seeded into areas of established introduced and native species. Hull and Klomp (1966) reported

crested wheatgrass exhibited continued high production

over a 33-year period. It persisted and even spread in some

locations under adverse conditions. This included: heavy

use, disease and extremes in temperature and moisture.

Additionally, Hull and Stewart (1948) found crested wheatgrass to survive and spread into stands of cheatgrass.

Pavlychenko and Kirk (1946) conducted a study to determine if crested wheatgrass could control perennial weeds on

dryland farms in Saskatchewan, Canada. Plots containing

well established stands of perennial sow thistle [Sonchus

arvensis L.], blue lettuce [Lactuca tatarticas L.], toad flax

[Linaria canadensis (L.) Dum.-Cours.], Canada thistle

Figure 2—Native herbaceous understory species

richness.

Figure 3—Native herbaceous understory species diversity.

5.9

3.3

p=0.022

Native Species

0

1

2

3

4

5

6

Non-Chained Chained

Diversity

11.4

10.5

p=0.570

Native Species

0

2

4

6

8

10

12

Chained Non-Chained

Richness
196 USDA Forest Service Proceedings RMRS-P-21. 2001

Vernon, Anderson, and Davis Response of Residual Native Species After Two-Way Chaining and Seeding in Utah

[Cirsium arvense (L.) Scop.], field bindweed [Convolvulus

arvense L.], leafy spurge [Euphorbia esula L.], poverty weed

[Iva axillaris L.], white top [Cardaria draba (L.) Desv.] and

Russian knapweed [Centaurea repens L.] were hand seeded

with crested wheatgrass at a rate of 28 kg/ha. After 5 years,

all plants of perennial sow thistle, blue lettuce, toad flax and

Canada thistle were eliminated from the plots. All other

species were greatly reduced with field bindweed showing

the least suppression. Crested wheatgrass was also recommended for seeding abandoned farmland occupied by Russian thistle [Salsola iberica A. Nels.] and tumble mustard

[Sisymbrium altissimum L.] by Reitz and others (1936).

Intermediate wheatgrass has similar traits as crested

wheatgrass with the exception that it is a sod former and is

not as drought tolerant. It is able to compete very well with

other species for resources and quickly established after

seeding on treatments in Utah (Plummer and others 1970).

Plummer and others (1970) also reported that a seed mixture containing crested wheatgrass, intermediate wheatgrass and Russian wildrye essentially eliminated cheatgrass

on a site in Central Utah. Similarly, Skousen and others

(1989) showed crested wheatgrass, intermediate wheatgrass and Russian wildrye to establish and persist over a

long period of time in the Intermountain region.

Plant nutrients are essential for plant communities to

establish and persist after treatment. Pinyon and juniper

trees that have invaded a site and are now dominant in

communities claim much of the water and nutrient resources that were previously used by the herbaceous species

(Doughty 1987). Tiedemann (1987) reported that invasion of

grass/forb and sagebrush/grass areas by pinyon and juniper

was accompanied by a greater nutrient accumulation in

Table 1—Significance of seeding variables on native herbaceous understory abundance

for chained pinyon-juniper woodlands in Utah.

Variable F-value Prob>F r2-value

Total seed lbs/acre 2.10 0.19 0.23

Total seed/m2 3.25 0.11 0.29

Grass seed/m2* 8.11 0.02 0.50

Proportion of crested wheatgrass in mix

 (seeds/m2

)

* 9.71 0.01 0.55

Proportion of intermediate wheatgrass

 in mix (seeds/m2

) 1.18 0.31 0.13

Proportion of crested and intermediate

 wheatgrass in mix (seeds/m2)

* 8.00 0.02 0.50

Crested wheatgrass abundance after

 treatment* 12.63 0.01 0.61

Intermediate wheatgrass abundance after

 treatment* 0.14 0.72 0.02

Crested and Intermediate wheatgrass

 abundance after treatment* 5.07 0.05 0.39

*

 Negatively associated with response variable.

Table 2—Significance of seeding variables on percent change in native herbaceous

species diversity (Shannon-Weiner Index) after treatment for chained pinyonjuniper woodlands in Utah.

Variable F-value Prob>F r2-value

Total seed lbs/acre 0.48 0.51 0.07

Total seed/m2* 0.00 0.99 0.00

Grass seed/m2* 1.08 0.33 0.12

Proportion of crested wheatgrass in mix

 (seeds/m2

)

* 2.59 0.15 0.25

Proportion of intermediate wheatgrass

 in mix (seeds/m2)

* 0.96 0.36 0.11

Proportion of crested and intermediate

 wheatgrass in mix (seeds/m2)

* 2.50 0.15 0.24

Crested wheatgrass abundance after

 treatment* 4.62 0.06 0.37

Intermediate wheatgrass abundance

 after treatment* 6.77 0.03 0.46

Crested and Intermediate wheatgrass

 abundance after treatment* 25.56 0.00 0.76

*

 Negatively associated with response variable.
USDA Forest Service Proceedings RMRS-P-21. 2001 197

Response of Residual Native Species After Two-Way Chaining and Seeding in Utah Vernon, Anderson, and Davis

aboveground biomass. The native woodland sites investigated in this study were considered to be mature with a lack

of herbaceous understory. Due to the lack of herbaceous

understory species and the associated poor seed bank, seeds

of exotic, perennial species were seeded during treatment to

enhance the herbaceous vegetation component. Resources

redistributed by removing the dominant pinyon-juniper

overstory would be available for seedling establishment and

plants that were present at the time of treatment. Exotic

species may benefit more than natives species due to the

shear abundance of exotic species seed on site. Furthermore,

aggressive species, such as crested and intermediate wheatgrass, would have an even greater advantage due to less

stringent germination requirements, more competitive seedlings and post-establishment competitiveness as compared

to native species. Not surprisingly, seeded species abundance (sum of nested frequency) was significantly greater

than native species abundance (66.5 and 17.1 respectively)

after treatment on the sites examined in this study.

Another factor perhaps influencing the significant difference in diversity and abundance between chained and nonchained sites may be site potential changes imposed by the

new assemblage of species on the treated sites. Several

studies suggest that there may be long term negative impacts by crested wheatgrass stands on soil. Lesica and

DeLuca (1999) provide a comprehensive review of literature

regarding soil changes that can be attributed to crested

wheatgrass stands in a mid-grass prairie. For instance,

crested wheatgrass stands have a lower below ground biomass than the native prairie grasses (Dormaar and others

1995; Smoliak and Dormaar 1985). This can lead to lower

energy input into the soil as compared to the native range

and alter physical and biochemical processes (Dormaar and

others 1978). Stands of crested wheatgrass are associated

with higher bulk density, fewer water stable aggregates and

lower levels of organic matter and nitrogen compared to

stands of native grasses (Redente and others 1989; Dormaar

and others 1978; Smoliak and others 1967). Crested wheatgrass also provides the soil with a relatively high concentration of carbohydrates and little organic nitrogen (Klein and

others 1988). Klein and others (1988) suggest that these

alterations to soil quality may prevent native species from

invading crested wheatgrass monocultures. Mid-grass prairies obviously have different soil and site potentials, but it is

worth pointing out the influences crested wheatgrass exhibits in some situations that were not examined in this

specific situation. Similar soil chemical and physical changes

may be occurring to soil in the Intermountain region after

chaining and seeding with crested wheatgrass and may be

restricting native species expansion or persistence.

Another influence listed by Walker and others (1995)

affecting the recovery of residual native species following

treatment is livestock and wildlife grazing. While livestock

access and utilization of treated sites can be somewhat

controlled, wildlife utilization, and its’ measurement, is

another matter.

Some variables that were presumed to influence native

species response prior to this study ultimately showed low

correlation. For instance, it was hypothesized that as time

passed since chaining, native species would increase in

density relative to when it was seeded. Our data indicate

that this is not the case as seeded species values were

similar for all sites regardless of time since treatment.

Similarly, Walker and others (1995) reported that although native grass abundance responded positively for

3 years following chaining, the native grasses slowly started

showing negative response and declined over time, presumably from competition with exotic grasses. They also

report that 23 years after chaining and seeding, the exotic

grasses became more dominant in the communities and

that plant dominance had not yet stabilized.

Seed mixes used in the revegetation projects examined in

this study varied with respect to total seeding rate and the

proportion of various species such as crested and intermediate wheatgrass within the mixture across all sites. One

objective of this study was to determine if variations of seed

mixtures affected native species diversity and abundance.

Data from this study indicated that both native species

abundance and diversity were significantly lower in the

chained plots versus the non-chained plots. However, these

differences were best correlated with the abundance of

crested and intermediate wheatgrass after chaining and

seeding rather than the specific seed mixtures used on the

sites. This raised the question whether a correlation exists

between the seed mixes used on these sites and the resulting

abundance of species following treatment. If a significant

correlation existed, seed mixes might be tailored for improved native species response.

Regression analysis showed low association between proportions of species in the seed mixes and the relative abundance of crested and intermediate wheatgrass after treatment. These results are similar to those of Davis and Harper

(1990). They reported that it is difficult to maintain a stand

of specified composition after treatment because each species responds differently to natural and imposed environmental factors. Pyke (1995) also points out that although

many species are included in a seed mix, establishment and

persistence of each species depends on many biotic and

abiotic factors. With this in mind, it should not be surprising

that the assemblage of plants on a site would not necessarily

correlate to the seed mix applied to the site and would vary

through time in response to various external factors.

The judgement of success or failure of the treatments

reviewed in this study should not be solely based on the

diversity or abundance of native species following treatment. The goals and objectives for the revegetation projects

examined in this study were generally to protect the soil

resource, increase forage for livestock and/or restore big

game ranges; not to enhance native species diversity or

abundance. The approach used by these land managers was

to get desirable plants, whether they be exotic or native, to

establish under arid conditions following chaining pinyonjuniper woodlands. If increasing native species diversity or

abundance is to be considered an objective in the future, this

study indicates that a different approach than previously

used should be taken on sites similar to those examined in

this study.

Conclusions____________________

Native species diversity and abundance were significantly

lower after chaining and seeding. Varying combinations of

introduced species in the seed mix showed some association

with the resulting native herbaceous understory diversity
198 USDA Forest Service Proceedings RMRS-P-21. 2001

Vernon, Anderson, and Davis Response of Residual Native Species After Two-Way Chaining and Seeding in Utah

and abundance. However, post-treatment abundance of

crested and intermediate wheatgrass combined was the best

indicator of native herbaceous understory diversity. This

association was negative. Although this may lead one to

believe that if the proportion of crested and intermediate

wheatgrass were decreased in the seed mix, the abundance

of these species after treatment would decrease as well. This

was not the case as the proportion of crested and intermediate seeds in the seed mix had low correlation with crested

and intermediate wheatgrass abundance at the point in

time when these sites were sampled.

Inclusion of adapted native species in the seed mix in

conjunction with decreased proportions of introduced species may be one alternative to enhance the native species

community after treatment. This does not necessarily mean

excluding exotic species from seed mixes entirely, but determining the correct balance of exotic and native species.

Because site potential is potentially altered after pinyonjuniper invasion and the ensuing treatment, native species

alone in a seed mix may be inadequate to satisfy desired

goals or objectives, especially in light of the abundance of

invasive annual and secondary perennial weeds spreading

throughout the Intermountain West. Initially, protection of

the site may be the prudent course of action with follow up

treatments designed to increase native species diversity.

Acknowledgment _______________

Funding for this project was provided through Federal Aid

Grants W-82-R and W-135-R.

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200 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Stanley G. Kitchen is a Botanist and Gary L. Jorgensen is a Range

Technician, U.S. Department of Agriculture, Forest Service, Rocky Mountain

Research Station, Shrub Sciences Laboratory, Provo, UT 84606.

Abstract—Winterfat (Ceratoides lanata) is a long-lived shrub

with excellent drought tolerance and good to moderate tolerance

for herbivory. It often occurs as near monocultures in deep finetextured soils of alluvial fans and valley bottoms. Winterfat communities are second only to those of shadscale (Atriplex confertifolia)

in dominance of the 16 million ha of salt-desert shrublands found

in Western North America. In spite of improved grazing practices,

winterfat is declining in many areas of the Great Basin. The

Eurasian summer annual, halogeton (Halogeton glomeratus), is

well adapted to the soils and climate associated with winterfat

communities and is invasive, replacing winterfat on degraded

sites. Recolonization of halogeton stands by winterfat is rare.

Subsequently, distinct winterfat- and halogeton-dominated communities often occur side by side. At the Desert Experimental

Range (Utah), episodic winterfat mortality at the ecotone has been

observed particularly after flood events and periods of higher than

average precipitation. The upward translocation and accumulation of cations, particularly sodium, in the soil by halogeton may

account, at least in part, for the lack of winterfat establishment in

halogeton stands. Other evidence suggests that a possible halogeton-induced change in soil microbiota may also be unfavorable for

winterfat. The development of viable management options to

restore winterfat communities will require a greater understanding of plant-soil interactions for these species.

Winterfat_______________________

Winterfat, or white sage (Ceratoides lanata), is a longlived short- to medium-statured chenopod shrub with excellent drought tolerance (Chambers and Norton 1993) due in

part to an extensive fibrous root system and deep penetrating taproot (Stevens and others 1977). It occurs in near

monocultures on fine textured lacustrine deposits found in

dry valley bottoms and as a more or less primary component

of mixed communities on deep alluvium derived from calcareous substrate. Until recent decades, winterfat dominated

the ‘island’ communities associated with rodent burrow

clusters, which are scattered within otherwise mixed shrub/

grass communities of valley alluvium (Kitchen and Jorgensen

1999).

Winterfat Decline and Halogeton Spread

in the Great Basin

Stanley G. Kitchen

Gary L. Jorgensen

Winterfat communities are second only to those of

shadscale (Atriplex confertifolia) in dominance of the 16

million ha of North American salt-desert shrubland found

primarily in the Great Basin (Blaisdell and Holmgren

1984). Common native associates include shadscale,

budsage (Artemisia spinescens), low rabbitbrush

(Chrysothamnus greenei), black sagebrush (Artemisia nova),

Indian ricegrass (Oryzopsis hymenoides), galleta (Hilaria

jamesii), and gooseberryleaf globemallow (Sphaeralcea

grossulariifolia). Within the context of currently accepted

models incorporating multiple stable states, successional

pathways, and interstate thresholds (Friedel 1991; Laycock

1991), a species that is represented in multiple stable

states might be safely considered late seral. Winterfat is

such a species (Comstock and Ehleringer 1992). Consistent

with a late seral strategy (Grime 1977; Tilman 1988) are

winterfat traits of plant longevity (Chambers and Norton

1993), inconsistent seed production (Blaisdell and Holmgren

1984), and absence of seed dormancy mechanisms necessary to preserve a soil seed reserve (Stevens and others

1977; Kitchen and Jorgensen 1999). It is, therefore, no

surprise that winterfat stands are slow to rebound following disturbance.

Winterfat is palatable and provides nutritious forage for

wildlife and livestock in all seasons. Although moderately

tolerant of herbivory (Harper and others 1990; Chambers

and Norton 1993), significant Great Basin reductions in

winterfat are attributed to abusive grazing practices by

domestic livestock from the 1870s to the 1930s, and later in

some locations (for example, Murdock and Welsh 1971).

Winterfat is most susceptible to grazing damage during

spring months when physiological activity is greatest

(Blaisdell and Holmgren 1984; Harper and others 1990). On

many locations, the condition of winterfat communities

improved somewhat as grazing frequency and intensity

were reduced consistent with implementation of the Taylor

Grazing Act of 1934. However, despite improved grazing

practices, Great Basin winterfat communities today show

patterns of continued, or perhaps, renewed decline (Harper

and others 1990; Alzerreca-Angelo and others 1998; Kitchen

and Jorgensen 1999).

Halogeton______________________

Halogeton, (Halogeton glomeratus) is a succulent halophytic annual native to central and southwestern Asia and

southeastern Europe. It is a prolific seed producer, even

under drought stress (Eckert 1954). Tisdale and Zappetini

(1953) reported yields of 25,000 seeds for larger plants and

800 seeds per plant in crowded stands where plant maturation height was only 76 mm. They found that vigorous stands
USDA Forest Service Proceedings RMRS-P-21. 2001 201

Winterfat Decline and Halogeton Spread in the Great Basin Kitchen and Jorgensen

produced from 220 to 450 kg of seed per ha. Halogeton seed

are small (1 to 2 million per kg) and easily dispersed by wind,

animal vectors, and vehicles. The production of both nondormant/short-lived black seed and dormant/long-lived brown

seed (Cronin and Williams 1966) provides the means for

both rapid spread and long-term persistence.

Although the timing and mode of introduction to the

United States are unknown, the first documented collection

of halogeton was made near Wells, Nevada, in 1934 (Dayton

1951). Although a weak competitor in perennial communities (Eckert 1954; Blaisdell and Holmgren 1984), this weed

is well adapted to the soils and climate associated with saltdesert shrublands and is quick to invade disturbed sites,

often resulting in near monocultures. Natural spread is

facilitated by human-caused disturbances, in particular, the

inadvertent creation of invasion corridors produced by road

construction and maintenance activities (Dayton 1951;

Stoddart and others 1951). After introduction, halogeton

spread rapidly through the overgrazed rangelands of the

semiarid West, infesting 4 million ha in the Western United

States within 30 years of first collection (Cronin and Williams

1966). Once a salt-desert shrubland community is converted

to halogeton, natural regeneration of native shrubs, such as

winterfat, generally does not occur (Eckert 1954; Harper

and others 1996).

The poisonous nature of halogeton for all classes of livestock, but more particularly for domestic sheep, was first

recognized in 1942 (Dayton 1951). This awareness, in combination with the rapid rate of spread that was observed,

captured the attention of the western range management

community and resulted in substantial research effort on

various aspects of halogeton biology during the 1940s and

1950s. One focus of that research was to examine the effect

of halogeton litter on the chemical and physical properties

of salt-desert soils. Eckert and Kinsinger (1960) conducted

controlled studies using Nevada soils collected from three

salt-desert community types and multiple levels of halogeton mulch. They demonstrated that the primary effect of

halogeton leachate was an increase in cations, primarily

sodium, at or near the soil surface with corresponding

increases in soil pH and electrical conductivity. Secondary

effects associated with the chemical changes included changes

in soil physical properties, including increased crust strength

and decreased percolation rate, and capillary rise of water

associated with halogeton soils.

Today, halogeton stands are common on sites previously

occupied by winterfat and are often found adjacent to remnant winterfat communities throughout the Great Basin.

Using 1998 and 1999 road surveys in central and eastern

Nevada and western Utah, we observed moderate to extensive displacement of winterfat by introduced annuals

(primarily halogeton) in 16 central Great Basin drainage

systems: specifically, Jakes, Monitor, Newark, Railroad,

Spring, Steptoe, and White River Valleys of central and

western Nevada, and Antelope, Escalante, Ferguson Desert,

Pine, Rush, Sevier Desert, Snake, Tule, and Wah Wah

Valleys of western Utah. Displacement had occurred in both

low-diversity valley bottom communities and in the ‘island’

vegetation associated with rodent burrow clusters scattered

in the more diverse alluvial community types. We concluded

that the probability of surveying winterfat habitat in the

Great Basin without observing significant displacement by

halogeton was probably quite low. Goodrich (2000) reported

a similar phenomenon in the Green River Basin of southwestern Wyoming, where halogeton is replacing stands of

Gardner saltbush (Atriplex gardneri). It is apparent that a

complete list of impacted communities will require additional reconnaissance.

Desert Experimental Range _______

In 1933, President Herbert Hoover set aside as an “agricultural range and experiment station” 22,500 ha (87 sections) located in western Millard County, Utah (Clary and

Holmgren 1982). Pastures and reference areas of the Desert

Experimental Range (DER), the Station’s current name,

were soon fenced for use in grazing and ecological studies,

which continue to the present. Today, research and monitoring activities at the DER are coordinated by the Forest

Service, Rocky Mountain Research Station, under the care

of the Shrub Sciences Laboratory in Provo, Utah.

The DER is located primarily within the northwest quarter of Pine Valley, a north/south trending closed basin with

a bottom elevation of 1,547 m and with several surrounding

peaks ranging from 2,400 to 2,900 m elevation. During the

late Pleistocene, the valley held a small lake with a maximum size of approximately 10,600 ha and an upper shore

line at about 1,570 m (Snyder and others 1964). A mostly

barren playa and remnants of old shorelines are the most

visible evidence of the lake.

Approximately 75 percent of the DER is coalescing alluvial fans, or bajadas, and valley bottom, including about half

of the playa. The remainder is steeper uplands and outcrops

made primarily of Paleozoic limestone and dolomite with

lesser amounts of quartzite and early tertiary volcanics.

Soils are mostly gravelly loams, sandy loams, and gravelly

sandy loams (Aridisols and Entisols; Tew and others 1997).

Soil series located on alluvium above ancient shorelines are

deep to very deep, with rapid to moderate permeability, and

moderate to well developed calcic horizons (Tew and others

1997). Soil series below these shorelines are very deep, with

moderate to moderately slow permeability and high levels of

exchangeable sodium (15 to 40 percent) in subsurface horizons (below 40 cm).

Precipitation at the DER is highly variable within and

between years. Mean annual precipitation at the headquarters complex (1,600 m) for the period of 1934 to 1981 was

157 mm with approximately half occurring from October

through April (Clary and Holmgren 1982). Annual precipitation for the last 25 years (1975 to 1999) averaged near

200 mm (Alzerreca-Angelo and others 1998; data on file at

the U.S. Forest Service, Shrub Sciences Laboratory, Provo,

Utah). Mean temperatures for January and July are –3.5

and 23.3 °C, respectively.

Vegetation on alluvial fans is salt-desert shrubland

with shadscale, winterfat, low rabbitbrush, bud sagebrush, Nevada ephedra (Ephedra nevadensis), and various

perennial grasses and forbs dominating. Multi-scaled patchiness in the vegetative matrix reveals variability in species

dominance, a reflection of the heterogeneity in soil composition, structure, and disturbance. Valley bottom vegetation is less diverse than that found on alluvial fans

(Kitchen and others 1999) and is comprised primarily of
202 USDA Forest Service Proceedings RMRS-P-21. 2001

Kitchen and Jorgensen Winterfat Decline and Halogeton Spread in the Great Basin

winterfat (sometimes in near monocultures), Indian ricegrass,

gray molly (Kochia americana), Bonneville saltbush (Atriplex

bonnevillensis), and halogeton. Black greasewood (Sarcobatus vermiculatus) and Nuttall saltbush (Atriplex falcata) are

conspicuous additions on colonized portions of the playa.

Halogeton Research at the Desert

Experimental Range _____________

The early history of halogeton at the DER is recorded in

unpublished documents on file at the U.S. Forest Service,

Shrub Sciences Laboratory, Provo, Utah, and is summarized

here. Halogeton was first observed at the DER in 1952 as a

small (approximately 1 ha) patch near the playa. At the time,

populations were known to exist in all basins surrounding

Pine Valley. Although the means of seed transport to the

DER is unknown, it was believed that seed might have come

by way of contaminated bales of hay dropped as emergency

feed in the winter of 1948 and 1949. A monitoring plan was

developed to assess the condition of this population as well

as to survey the remainder of the DER for new infestations

in coming years. New populations were identified in 1953

both inside and near DER boundaries. Small plots with and

without perennial vegetation were seeded to halogeton in

June of 1954 to assess establishment with and without

competition from perennials. Halogeton plants grew in all

plots the same year. During the next 4 years, halogeton

spread in Pine Valley from an increasingly greater number

of source populations. Subsequently, by 1958 halogeton was

widespread at the DER and surrounding lands. Within the

DER, halogeton was concentrated mostly within the more

open communities near the playa and on upland communities associated primarily with disturbance (rodent diggings,

roads, and so forth).

Boundaries between nearly pure stands of winterfat and

halogeton are generally well defined by a rather narrow

ecotone. This results from the inability of winterfat to invade

halogeton stands and the weak competitive attributes of

halogeton in healthy perennial communities. At the DER, no

natural regeneration of winterfat has occurred for up to 30

years following conversion to halogeton. However, halogeton advances have been observed following unexplained

winterfat die-off events preceded by either summer flooding

(Harper and others 1996) or extended periods of abnormally

high precipitation.

Harper and others (1996) observed changes in soil chemistry associated with halogeton conversion at the DER

similar to those observed in Nevada (Eckert and Kinsinger

1960). They also found evidence that halogeton conversion

had altered the soil microbial community as was predicted

by Eckert and Kinsinger. In greenhouse experiments

using treated (methyl bromide fumigation) and untreated

soils collected from the halogeton and winterfat communities, winterfat seedling survival in treated halogeton soil

(50.3 percent) was significantly higher than that for untreated halogeton soil (36.6 percent) and not significantly

different than that of treated (55.9 percent) and untreated

(47.4 percent) winterfat soils. These results suggest possible enhanced pathogenic activity associated with halogeton soils.

In 1998, additional soil samples were taken at four DER

sites near the playa. Samples were collected from adjoining

winterfat and halogeton stands, the ecotone between the

stands, and bare areas (<1 percent cover) located within

halogeton stands. These bare areas had supported solid

stands of halogeton in 1997 as determined by the condition

of standing litter. Three replicated samples were taken from

the top 10 cm for each site/plant community combination

(n = 12). Increases in sodium associated with halogeton

(table 1) were consistent with that reported by Eckert and

Kinsinger (1960) and Harper and others (1996). Halogeton-related increases in potassium and magnesium were

also significant. Our results also show that, although exchangeable concentrations of these cations were not significantly higher at the ecotone than in the winterfat community, they were trending upward and clearly were being

affected by halogeton litter. Change in cation concentration

between halogeton and winterfat soils, when expressed as a

ratio, was greater for sodium (3.7:1) than for potassium

(2.3:1) or magnesium (1.3:1). Eckert and Kinsinger (1960)

suggested that disproportionate increases in sodium could

cause reduced uptake of other cations resulting in nutrient

stress for affected plants. Whether by the direct affect of

increased sodium on plant growth, negative alteration of the

physical properties of soils, disruption of soil micro flora,

changes of cation ratios, or some combination of the above,

halogeton is clearly effective at rendering intolerable, soils

previously occupied by winterfat.

Because of the cumulative nature of these soil-chemistry

changes, it seems reasonable to assume that the length of

time a site is occupied by halogeton and the chemical,

physical, and perhaps biological condition of that soil as it

pertains to winterfat growth are inversely related. We believe that this is largely true, at least until conditions are so

poor that halogeton growth also becomes restricted. It is

possible that this occurred on the bare areas we observed at

the DER in 1998. Cation concentrations were clearly greater

in these soils than in other soils tested, including those

associated with dense halogeton stands (table 1). Interestingly, a full and vigorous stand of halogeton grew on the

previously bare areas in 1999. The 1998 boundary between

the halogeton stand and bare ground remained clearly

visible due largely to greater stand vigor (height, color,

biomass) associated with previously bare areas. This would

Table 1—Exchangeable concentrations (ppm) for four cations in top 10

cm of soil in adjoining winterfat and halogeton communities,

ecotone, and bare areas at four sites on the Desert

Experimental Range, Millard County, Utah (1998). Within

columns, means followed by the same letter are not

significantly different at the p < 0.05 level (SNK).

Community type Ca Mg K Na

- - - - - - - - - - - - - - - ppm - - - - - - - - - - - - - - -

Winterfat 8,736a 490c 636c 102c

Ecotone 8,359b 509c 793c 149c

Halogeton 8,371b 650b 1,455b 373b

Bare 8,644a 725a 1,633a 450a
USDA Forest Service Proceedings RMRS-P-21. 2001 203

Winterfat Decline and Halogeton Spread in the Great Basin Kitchen and Jorgensen

seem to suggest that halogeton rendered these sites unfavorable for halogeton (or most any other species present),

and that it remained so until soil conditions improved. For

example, the above average precipitation that occurred in

1998 (215 mm) could have been sufficient to partially leach

salts from near the soil surface, improving conditions on

bare soils. At the same time, such improvements might not

have occurred on soils with active halogeton stands due to

the extra halogeton biomass (and, therefore, salted litter)

produced in response to abundant soil water. Research that

could document and quantify this hypothesis has not been

done.

Conclusion_____________________

Winterfat decline is widespread in Great Basin salt-desert

communities. Presently, our knowledge of the processes by

which introduced annuals, particularly halogeton, displace

and exclude winterfat is deficient. Before we can assess the

probable effectiveness of potential management strategies

in preventing continued expansion of halogeton and in

restoring winterfat community stability, a more complete

understanding of interactions among winterfat and halogeton and associated soils and soil microbiota must first be

developed. Failure to respond to this challenge will likely

result in further degradation of winterfat-dominated communities in the Great Basin.

References _____________________

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Great Basin and Colorado Plateau. Great Basin Naturalist

52:195–215.

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Dayton, W. A. 1951. Historical sketch of barilla (Halogeton

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Eckert, R. E., Jr. 1954. A study of competition between whitesage

and halogeton in Nevada. J. Range Manage. 7:223–225.

Eckert, R. E., Jr.; Kinsinger, F. E. 1960. Effects of Halogeton

glomeratus leachate on chemical and physical characteristics of

soils. Ecology 41:764–772.

Friedel, M. H. 1991. Range condition assessment and the concept of

thresholds: a viewpoint. J. Range Manage. 44:422–426.

Goodrich, S. 2000. [Personal communication]. Vernal, Utah: U.S.

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Harper, K. T.; Van Buren, R.; Kitchen, S. G. 1996. Invasion of alien

annuals and ecological consequences in salt desert shrublands of

western Utah. In: Barrow, J. R.; McArthur, E. D.; Sosebee, R. E.;

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over a 54-year period in shadscale desert, west-central Utah. In:

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comps. Proceedings, symposium on cheatgrass invasion, shrub

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Kitchen, S. G.; Jorgensen, G. L. 1999. Annualization of rodent

burrow clusters and winterfat decline in a salt-desert community. In: McArthur, E. D.; Ostler, W. K.; Wambolt, C. L., comps.

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59–65.

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Valleys, western Utah. Science Bulletin, Biological Series,

Brigham Young University, vol. 12(4). 25 p.

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the Great Basin. Miscellaneous Geologic Investigations Map I416. Washington, DC: U.S. Geological Survey.

Stevens, R.; Giunta, B. C.; Jorgensen, K. R.; Plummer, A. P. 1977.

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No. 77-2. 41 p.

Stoddart, L. A.; Clegg, H.; Markham, B. S.; Stewart, G. 1951. The

halogeton problem on Utah’s Ranges. J. Range Manage. 4:223–227.

Tew, R. K.; Kitchen, S. G.; Holmgren, R. C. 1997. Soil survey—

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Rocky Mountain Research Station. 22 p.

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360 p.

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In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Robin E. Durham is a Graduate Student and Benjamin A. Zamora is a

Professor of Range Ecology in the Department of Natural Resource Sciences,

Washington State University, Pullman, WA 99164. Michael R. Sackschewsky

is a Senior Research Scientist in the Ecology Group and Jason C. Ritter is a

Science Associate in the Hydrology Group, Pacific Northwest National Laboratory, Richland, WA 99352. Support for this project was received from the

U.S. Department of Energy under Contract DE-AC06-76RLO 1830.

Predicting First-Year Bare-Root Seedling

Establishment With Soil and Community

Dominance Factors

Robin E. Durham

Benjamin A. Zamora

Michael R. Sackschewsky

Jason C. Ritter

Abstract—The usefulness of measuring community dominance

factors and the soil parameters of geometric mean particle size and

percent fines as predictors of first-year bare-root establishment of

Wyoming big sagebrush seedlings was investigated. The study was

conducted on six sandy soils in south-central Washington. Soil

parameters that could affect the distribution of Sandberg’s bluegrass and cheatgrass as dominants in seral plant communities were

also examined. Plant health was inversely related to increasing

geometric mean particle size and directly related to increasing

percent fines. Percent fines were also directly related to cheatgrass

cover on these sandy soils. The highest sagebrush survival occurred

on the alien-dominated sites.

Introduction ____________________

Mitigation for impacts to mature sagebrush habitat on the

Hanford Site was conducted during fall 1998 on the semiarid

sagebrush steppe of south-central Washington. Restoration

in this area usually relies in part on transplanting Wyoming

big sagebrush (Artemisia tridentatassp. wyomingensisBeetle

& Young) seedlings into post fire habitats where the shrub

component is absent. Bare-root seedlings are inexpensive to

produce and plant, and have been shown to establish as

readily as container-grown stock under good conditions

(Whisenant 1999). However, bare-root seedling establishment in poor or more variable conditions has not been as

successful (Barnett and McGilvray 1997; McKell and Van

Epps 1980; Lohmiller and Young 1972). In conjunction with

the 1998 habitat mitigation effort, a field study was initiated

to investigate environmental and vegetational elements of

the landscape that might be associated with successful

establishment of bare-root seedlings. This research was

conducted in the Lower Cold Creek valley on the Fitzner/

Eberhardt Arid Lands Ecology Reserve (ALE) adjacent

to the Department of Energy’s (DOE) Hanford nuclear

reservation.

Landscapes are sometimes described as a blend of resource patches that support a mosaic of plant communities

associated with changes in slope, aspect, and soil type

(Whisenant 1999). In the sagebrush steppe of south-central

Washington, resource patches are often the result of soil

water availability, which is one of the most significant

edaphic features affecting the distribution of habitat types

across this semiarid landscape (Daubenmire 1974; Franklin

and Dyrness 1988; Hironaka 1979).

Soils with high water holding capacity allow plants to

survive periods of drought (Larcher 1995). While temporary

physiologically induced water deficits often occur mid day

when it is hot and sunny, long-term deficits are mainly

caused by decreasing soil water availability (Kramer 1983).

As the water content within the root zone decreases, the

remaining water becomes less available to plants (Bristow

and others 1984; Larcher 1995). The degree to which this

availability is limited is strongly dependent on the soil’s

texture, or particle size distribution (Larcher 1995). Coarse

sandy soils exhibit a low affinity to water (which makes it

easier for plants to obtain); however, they also have a low

water holding capacity. This is evident as farmers are forced

to irrigate at much higher (less negative) soil water potentials in sands than in silts or clays (Bristow and others 1984).

It is reasonable to expect that planted seedlings would be

affected by environmental gradients. Because shrub transplanting can be expensive, careful site selection that considers these gradients is an important and reasonable approach

to achieving a high level of success.

Shiozawa and Campbell (1991) have shown that soil

texture in terms of a geometric mean particle diameter and

a geometric standard deviation are associated with the soil

hydraulic property of moisture retention. If a significant

association exists between geometric mean particle diameter and first-year seedling establishment, then these modeled parameters could be useful in selecting appropriate

sites for planting in sandy areas.

Community competition on a site may also be a factor to

consider in the prediction of restoration success. One of the

more prominent plant species across the study area is

cheatgrass (Bromus tectorum L.). While this ubiquitous

winter annual maintains a competitive edge across most of

the study area, its distribution and abundance varies in

response to environmental gradients (Rickard 1975). Across
USDA Forest Service Proceedings RMRS-P-21. 2001 205

Predicting First-Year Bare-Root Seedling Establishment With Soil and Community Dominance Factors Durham, Zamora, Sackschewsky, and Ritter

much of the lower elevations of Hanford and ALE, cheatgrass has replaced the small native bunchgrass, Sandberg’s

bluegrass (Poa secunda Presl.), as the dominant understory

species (Daubenmire 1970; Rickard 1975), yet Sandberg’s

bluegrass is still found to dominate or co-dominate on this

habitat type in many areas. Link and others (1990) determined that the dominance of one or the other of these species

was not a direct result of phenological differences or plant

water status, but suggested it might depend on some other

abiotic or biotic factors.

The purpose of this study was to find a practical approach

to the prediction of bare-root seedling establishment on

sandy sites in varying competitive environments, and to

investigate the soil parameters that might be affecting the

distribution of Sandberg’s bluegrass and cheatgrass as dominants in seral plant communities on the Wyoming big

sagebrush/Sandberg’s bluegrass habitat type. The specific

objectives were to characterize the relationships that exist

between: (1) modeled geometric mean particle sizes and

corresponding percent fines (percentage of particle sizes less

than 53 μm) to first-year survival and health of bare-root

Wyoming big sagebrush seedlings; (2) modeled geometric

mean particle sizes and percent fines to community composition; and (3) community composition to first-year bare-root

seedling survival.

Methods _______________________

Six 20-m x 30-m study plots were positioned on ALE along

a sandy drainage of the Lower Cold Creek valley. The sites

were in a post-burn seral condition with the shrub component lacking due to fire. The sites had not burned in at least

10 years. Three sites (A1, A2, A3) were selected to represent

alien communities dominated by cheatgrass, while three

other sites (N1, N2, N3) were selected to represent native

communities dominated by Sandberg’s bluegrass. Elevation

at the study sites is about 134 m (440 ft). The potential native

vegetation is Wyoming big sagebrush/Sandberg’s bluegrass.

Normal effective precipitation (October through May) is

126 mm (4.9 inches), with summer precipitation averaging

33 mm (1.3 inches) at the Hanford Meteorological Station

(HMS) located about 22.5 km (14 mi) NNW of the study areas

(Hoitink and others 1999). The soils were mapped into the

Burbank series, which is made up of coarse-textured sands

and loamy sands underlain by gravel (Hajek 1966).

Soil Measurements

Soils were sampled systematically at each site. Five cores

were extracted at two depths (0.3 m and 1.0 m respectively)

from each site. Samples from each core (30 cores, 60 samples)

were sent to Soiltest Farm Consultants in Moses Lake,

Washington, where nutrient content, soluble salts, organic

matter, pH, and cation exchange capacities (CEC) were

determined. Sand, silt and clay fractions were determined

using hydrometer and wet sieve methods (Gee and Bauder

1986) on the 0.3-m soil samples. Prior to hydrometer measurements, soil samples were soaked in sodiumhexametaphosphate solution and placed on a shaker table

overnight for particle dispersion. Soil drying methods and

soil water calculations were conducted following Gardner (1986).

The parameters of geometric mean particle diameter and

the associated standard deviation were estimated based on

the two-parameter Sirazi and Boersma (SB) model described by Shiozawa and Campbell (1991):

dg = exp(5.756 – 3.454mt – 7.712my) (1)

and,

 

σ g t yg = [ ] −−− m md ( ) 









 exp . . . ln /

33 14 27 84 29 31 2 1 2

(2)

where: dg is the geometric mean particle diameter, σg is the

geometric standard deviation (both in μm), and the silt and

clay fractions are represented by mt and my respectively.

Community Measurements

Percent cover, species composition (based on relative

cover), and frequency were determined during May 1999,

following the coverage class method described by Daubenmire

(1959), using a modified 0.2-m x 0.5-m sampling frame. Fifty

samples were obtained from each site by splitting the

20-m x 30-m planting areas into two 10-m x 30-m halves. Five

10-m lines were then randomly positioned along the interior

long axis and the flip of a coin determined if the lines would

be positioned to the left or right of the tape. The sampling

frame was then systematically positioned every meter along

each of the five lines and ocular estimates of percent cover,

percent species composition, and percent frequency for each

species were determined.

Seedling Measurements

During November 1998, each 20-m x 30-m planting area

was divided into 120 sections. Bare-root seedlings were

randomly assigned (60 at each site) within each planting

area. Seedling roots were dipped into a solution of water and

fine-grade Terra-SorbTM hydrogel (acrylamide coploymer)

before planting. The following summer, during late July

1999, plant survival and health were qualitatively ranked

according to the plant’s overall appearance and phenological

development (Caldwell and others 1973; Daubenmire 1975),

and the following guidelines:

0 Dead, no live leaves left on the plant.

1 Plant displays low vigor (for example, no apparent new

growth, no bud or reproductive stem elongation, and so

forth) and at least 61 percent of the foliage is missing,

chlorotic, or otherwise unhealthy in appearance.

2 Plant displays good vigor (for example, new growth and

relatively green turgid leaves) and only displays between 11 and 60 percent of the unhealthy characteristics listed above.

3 Plant displays very good vigor (for example, ephemeral

leaves growing on reproductive shoots) and displays no

more than 10 percent of the unhealthy characteristics

listed above.

All seedlings were identified (alive or dead), and measures of

seedling height and two widths were recorded. Data for

second-year survival, health, and growth, were not obtained

because the test sites were destroyed by a large range fire

that occurred in June 2000.
206 USDA Forest Service Proceedings RMRS-P-21. 2001

Durham, Zamora, Sackschewsky, and Ritter Predicting First-Year Bare-Root Seedling Establishment With Soil and Community Dominance Factors

Analysis

Logistic regression and analysis of deviance were used to

analyze the relationship between environmental and community characters and the multinomial ordinal response of

the bare-root seedlings. The SAS Genmod procedure (SAS

Institute, Cary, North Carolina) was used to perform the

calculations.

Results and Discussion __________

Effective precipitation recorded at the HMS for the 1998–

1999 (October through May) growing season totaled 99 mm

(3.9 inches), which is about 78 percent of normal (Hoitink

and others 1999, 2000). Summer precipitation received

during the two months prior to seedling health and survival

measurements totaled 10 mm (0.38 inches).

Soil and Seedling Measurements

Although there were several notable differences between

the soil properties of the alien study plots and the native study

plots (table 1), native plot N2 was more similar to the three

alien plots in terms of soil properties than to the other two

native plots. The alien plots exhibited higher percent fines

and lower geometric mean particle sizes, than the native

plots. In addition, alien plots had higher magnesium contents

and higher CEC than the native plots (table 1). All sampled

soils were considered alkaline, exhibiting pH values from 7.9

to 8.6 and increasing at depth to a maximum pH of 9.2. Soluble

salts were also low across all plots (0.2 dSm–1), indicating no

hinderance to plant growth (Cline and others 1977).

Modeled geometric mean particle size was related to plant

health (X2 = 13.41, p = 0.0003, df = 1). Plant survival was

inversely related to increasing geometric mean particle size

(fig. 1). Mean particle sizes ranged from 97.1 to 213.3 μm.

Modeled means across all sites were classified as fine sands

based on the USDA classification system.

Percent fines were also shown to be related to plant health

(X2 = 12.22, p = 0.0005, df = 1) with plant survival directly

associated with increasing percent fines (fig. 2). Percent

fines ranged from 5 to 27 percent. Seedling survival ranged

from 42 to 87 percent (figs. 1, 2, 3).

Soil and Community Measurements

Percent fines were directly related to cheatgrass cover

indicating that this component of soil texture was a good

predictor of community dominance in the samples measured

for this study (X2 = 245.83, p < 0.0001, df = 1). Lower

cheatgrass cover was observed on soils exhibiting less than

15 percent fines (tables 1 and 2). Nevertheless, native site

N2 was found on soils similar to the soils found on the aliendominated sites (table 1), indicating that community dominants on that site were affected by factors other than soil

texture and available water.

Table 1—Summary of selected physical and chemical properties measured on the six study sites. Data are presented as means with ± one standard

deviation (n = 5 soil cores from each site).

Alien-dominated plots Native-dominated plots

A1 A2 A3 N1 N2 N3

Texture

Percent sand 82.8 ± 1.7 70.6 ± 3.7 71.6 ± 1.0 94.3 ± 1.0 79.6 ± 5.0 89.8 ± 3.5

Percent fines 17.2 ± 1.7 29.4 ± 3.7 28.4 ± 1.0 5.7 ± 1.0 20.4 ± 5.0 10.2 ± 3.5

Mean particle size (μm) 126 ± 9.1 97 ± 7.4 106 ± 6.6 213 ± 5.2 134 ± 6.5 158 ± 9.0

Nutrients

Calcium (ppm) 964 ± 62.3 1136 ± 121 1136 ± 32.9 856 ± 388 1180 ± 130 764 ± 108

Magnesium (ppm) 174 ± 18.4 177 ± 38.8 186 ± 22 84.7 ± 24.2 201 ± 13.8 96.8 ± 28.4

Soluble salts (dSm–1)

0.3 m depth 0.20 ± 2E-09 0.26 ± 0.089 0.20 ± 2E-09 0.20 ± 2E-09 0.20 ± 2E-09 0.20 ± 2E-09

0.9 m depth 0.46 ± 0.358 0.22 ± 0.045 0.20 ± 2E-09 0.22 ± 0.045 0.30 ± 0.228 0.22 ± 2E-09

Cation exchange capacity

meq/100 g 6.5 ± 0.5 6.9 ± 0.5 7.0 ± 0.4 3.5 ± 0.5 7.2 ± 1.1 4.2 ± 0.3

pH 0.3 m depth 8.0 ± 0.1 8.4 ± 0.2 8.0 ± 0.2 8.2 ± 0.2 8.1 ± 0.2 8.4 ± 0.1

0.9 m depth 8.6 ± 0.5 9.2 ± 0.1 8.7 ± 0.4 8.7 ± 0.1 9.0 ± 0.1 8.9 ± 0.1

Figure 1—Percent survival of Wyoming big sagebrush seedlings relative to modeled geometric

mean particle diameters for the six study sites.

Bars represent ± one modeled standard deviation (n = 5 soil cores from each planting site).
USDA Forest Service Proceedings RMRS-P-21. 2001 207

Predicting First-Year Bare-Root Seedling Establishment With Soil and Community Dominance Factors Durham, Zamora, Sackschewsky, and Ritter

Sandberg’s bluegrass cover on the native sites was between

30 and 39 percent and fell between 0.3 and 11.6 percent on

the alien dominated sites. Likewise, cheatgrass cover on the

native sites was between 16 and 22 percent and reached

between 53 and 68 percent on the alien dominated sites. All

sites exhibited low species diversity (table 2) which is consistent with the Wyoming big sagebrush/Sandberg’s bluegrass

habitat type (Daubenmire 1970).

Conclusions____________________

Our study found that geometric mean particle size, percent fines, and community-dominance factors could be good

indicators of potential bare-root seedling survival. With

respect to soil texture, measuring geometric mean particle

size was cumbersome and time consuming. The percent

fines in a soil were much easier to measure, and can predict

seedling establishment success just as well. Based on this

data from the Lower Cold Creek valley, overall establishment success is more likely in soils containing greater than

15 percent fines. We recommend that percent fines, rather

than geometric mean particle size, be used as an indicator of

environments that would promote the successful establishment of bare-root seedlings on sandy locations. Furthermore, percent fines were found to be good predictors of

community dominance, and community dominance factors

were considered good predictors of seedling establishment.

Often site selection guidelines restrict mitigation areas to

high quality native sites. However, when quality native sites

are not available, or if successful establishment of sagebrush

is the only goal, the data provided in this study suggest that

cheatgrass stands on sandy sites can be indicative factors

that promote successful establishment of bare-root Wyoming big sagebrush seedlings.

Acknowledgments ______________

The authors wish to thank Jennifer Lewinsohn and Craig

McKinstry for their technical assistance during the preparation of this manuscript. We would also like to thank Beth

Maley, Von Whitney, Richard Langstaff, Pat Mueller,

MaryLee Strub, and Skip Shaw for their tireless help in the

field.

References _____________________

Barnett, J. P.; McGilvray, J. M. 1997. Practical guidelines for

producing longleaf pine seedlings in containers. Gen. Tech. Rep.

SRS-14. U.S. Department of Agriculture, Forest Service, Southern Research Station.

Bristow, K. L.; Campbell, G. S.; Calissendorff, C. 1984. The effects

of texture on the resistance to water movement within the

Rhizosphere. Soil Science Society of America Journal. 48(2):

266-270.

Caldwell, M. M.; Wiebe, H. H.; DePuit, E. J.; Fernandez, O.; Camp,

L. B.; Fareed, M. 1973. Gas exchange, translocation and root

growth of cold desert plants. US/IBP Desert Biome Res. Memo.

73-13. Logan: Utah State University. 41 p.

Cline, J. F.; Uresk, D. W.; Rickard, W. H. 1977. Plants and soil of a

sagebrush community on the Hanford Reservation. Northwest

Science. 51: 60-70.

Daubenmire, R. 1959. A canopy-coverage method of vegetational

analysis. Northwest Science. 33(1): 43-64.

Figure 2—Percent survival of Wyoming big sagebrush seedlings relative to the percent fines across

the six study sites. Bars represent ± one standard

deviation (n = 5 soil cores from each planting site).

Figure 3— Health rankings in relation to alien [A]

or native [N] dominated communities, texture,

percent fines, and geometric mean particle diameters across the six study sites. Data are ordered

by increasing survival (n = 60 bare-root Wyoming

big sagebrush seedlings planted at each site).

Textures were determined based on the USDA

classification scheme (s = sand, sl = sandy loam,

and ls = loamy sand).

Community and Seedling Measurements

Community factors of percent cover appear to be good

predictors of bare-root seedling survival on these sandy sites

(X2 = 7.12, p = 0.0076, df = 1). Overall, the highest sagebrush

survival occurred on the alien dominated sites with percent

survival ranging between 58 and 87 percent (figs. 1, 2, and

3). This may be due to the increased percent fines and

corresponding increased water-holding and cation-exchange

capacities. On native sites N1 and N3, sagebrush survival

was 42 and 45 percent respectively, while native site N2

exhibited an 82 percent survival (figs. 1, 2, and 3). Clear

distinctions were evident with respect to percent cover and

frequency between the native and alien plots (table 2).
208 USDA Forest Service Proceedings RMRS-P-21. 2001

Durham, Zamora, Sackschewsky, and Ritter Predicting First-Year Bare-Root Seedling Establishment With Soil and Community Dominance Factors

Table 2—Community measurements across the six study sites (n = 50, 0.2-m x 0.5-m plots from each 20-m x 30-m study site).

Alien dominated plots Native dominated plots

Taxa A1 A2 A3 N1 N2 N3

Shrubs Percent cover * Percent species composition * Percent frequency

Artemisia tridentata –1 – –– +2 +

Chrysothamnus nauseosus – – –– – +

Half shrubs

Phlox logifolia + – –– + +

Antennaria dimorpha – – –– + –

Native perennial grasses

Poa secunda 8.4 * 11.3 * 46 11.6 * 13.4 * 84 0.3 * 0.4 * 2 30.0 * 52.0 * 96 34.4 * 56.6 * 98 39.1 * 61.6 * 98

Pseudoroegneria spicatum – – –– + –

Sitanion hysterix ––– – 0.8 * 1.2 * 2 –

Stipa comata + – –+ – –

Stipa thurberiana ––– – 0.8 * 1.2 * 2 –

Introduced annual grasses

Bromus tectorum 53.0 * 71.7 * 100 67.6 * 76.7 * 100 62.6 * 83.0 * 100 16.0 * 27.7 * 82 21.9 * 36.0 * 96 18.9 * 29.7 * 96

Native perennial forbs

Balsamorhiza careyana – + –– + +

Chaenactis douglasii ––– – – 0.1 * 0.2 * 4

Crepis atrabarba – + –– + –

Erigeron poliospermus – – –– + +

Lomatium macrocarpum – – –– + –

Machaeranthera canescens – – –– + –

Native annual forbs

Agoseris heterophylla – 0.1 * 0.1 * 2.0 – – 0.8 * 1.2 * 2 –

Ambrosia acanthicarpa 0.3 * 0.3 * 10 – – – – 0.3 * 0.3 * 10

Amsinckia tessellata 0.1 * 0.1 * 2 – + 0.1 * 0.1 * 2 – –

Epilobium paniculatum 0.1 * 0.1 * 2 0.4 * 0.4 * 14 0.1 * 0.1 * 4 – – –

Microsteris gracilis ––– 0.1 * 0.1 * 2 – 0.1 * 0.2 * 4

Introduced annual forbs

Draba verna 0.8 * 1.1 * 32 3.9 * 4.4 * 86 4.3 * 5.7 * 62 8.4 * 14.6 * 96 1.1 * 1.8 * 44 3.6 * 5.6 * 54

Holosteum umbellatum 7.8 * 10.5 * 82 4.0 * 4.5 * 72 6.4 * 8.5 * 58 1.8 * 3.0 * 15 – 0.7 * 1.0 * 26

Salsola kali 1.9 * 2.5 * 54 0.5 * 0.6 * 20 0.7 * 0.9 * 26 1.2 * 2.0 * 46 1.2 * 3.5 * 48 0.3 * 0.5 * 12

Sisymbrium altissimum 1.3 * 1.8 * 22 0.1 * 0.1 * 2 0.2 * 0.3 * 8 0.2 * 0.3 * 6 – –

Tragopogon dubius 0.6 * 0.7 * 12 0.1 * 0.1 * 4 0.9 * 1.2 * 6 0.2 * 0.3 * 6 – +

Total native taxa and % cover 6 * 8.9% 6 * 12.1% 3 * 0.4% 4 * 30.2% 13 * 36.8% 10 * 39.6%

Total alien taxa and % cover 6 * 65.4% 6 * 76.2% 6 * 75.1% 6 * 27.8% 3 * 24.2% 5 * 23.5%

1– = not present on site.

2

+ = present but not sampled.

Daubenmire, R. F. 1970. Steppe vegetation of Washington. Tech.

Bull. 62. Pullman, WA: Washington State University, Experimental Station.

Daubenmire, R. F. 1974. Plants and environment; a textbook of

plant autecology. 3rd ed. New York: Wiley.

Franklin, J. F.; Dyrness, C. T. 1988. Natural vegetation of Oregon

and Washington. Corvallis: Oregon State University Press.

Gardner, W. H. 1986. Water content. In: Klute, A., ed. Methods of

soil analysis, Part 1-Physical and mineralogical methods. 2nd ed.

Madison, WI: American Society of Agronomy, Inc.

Gee, G. W.; Bauder, J. W. 1986. Particle-size analysis. In: Klute, A.,

ed. Methods of soil analysis, Part 1-Physical and mineralogical

methods. 2nd ed. Madison, WI: American Society of Agronomy,

Inc.

Hajek, B. F. 1966. Soil survey: Hanford Project in Benton County,

Washington. BNWL-234. Richland, WA: Pacific Northwest

Laboratories.

Hironaka, M. 1979. Basic synecological relationships of the Columbia River sagebrush type. Contribution No. 124. Moscow, ID:

University of Idaho, Forest, Wildlife and Range Experiment

Station.

Hoitink, D. J.; Burk, K. W.; Ramsdell, J. V. 1999. Hanford Site

climatological data summary 1998 with historical data. PNNL12087. Richland, WA: Pacific Northwest National Laboratory.

Hoitink, D. J.; Burk, K. W.; Ramsdell, J. V. 2000. Hanford Site

climatological data summary 1999 with historical data. PNNL13117. Richland, WA: Pacific Northwest National Laboratory.

Kramer, P. J.1983. Water relations of plants. New York: Academic

Press.

Larcher, W. 1995. Physiological plant ecology: ecophysiology

and stress physiology of functional groups. 3rd ed. New York:

Springer-Verlag.

Link, S. O.; Gee, G. W.; Downs, J. L. 1990. The effect of water stress

on phenological and ecophysiological characteristics of cheatgrass

and Sandberg’s bluegrass. Journal of Range Management. 43(6):

506-513.

Lohmiller, R. G.; Young, W. C. 1972. Propagation of shrubs in the

nursery. In: McKell, C. M.; Blaisdell, J. P.; Goodin, J. R., eds.

Wildland shrubs: their biology and utilization. Gen. Tech. Rep.

INT-1. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station:

349-358.
USDA Forest Service Proceedings RMRS-P-21. 2001 209

Predicting First-Year Bare-Root Seedling Establishment With Soil and Community Dominance Factors Durham, Zamora, Sackschewsky, and Ritter

McKell, C. M.; Van Epps, G. 1980. Vegetative rehabilitation of arid

land disturbed in the development of oil shale and coal. EPA6007-80-071. Cincinnati, OH: USEPA, Industrial Environmental

Research Laboratory.

Rickard, W. H. 1975. Vegetation of knob and kettle topography in

south-central Washington. Northwest Science. 49: 147-152.

Shiozawa, S.; Campbell, G. S. 1991. On the calculation of mean

particle diameter and standard deviation from sand, silt, and clay

fractions. Soil Science. 152(6): 427-431.

Whisenant, S. G. 1999. Repairing damaged wildlands: a processorientated, landscape-scale approach. New York: Cambridge

University Press.
210 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Blair L. Waldron is a Research Geneticist, N. Jerry Chatterton is a

Research Plant Physiologist, and Burke W. Davenport is a Range Scientist at

the Forage and Range Research Laboratory, USDA-ARS, Logan, UT 84322-

6300. R. Deane Harrison is a Range Scientist (emeritus) at the Utah State

Agriculture Experiment Station, Forage and Range Research Laboratory,

USDA-ARS, Logan, UT 84322-6300.

Forage Kochia: Friend or Foe

Blair L. Waldron

R. Deane Harrison

N. Jerry Chatterton

Burke W. Davenport

Abstract—Perennial forage kochia (Kochia prostrata) is a halfshrub valuable for reclamation, fire breaks, and livestock and

wildlife forage on semiarid and saline rangelands. Interest is mounting about this species, but some are concerned that it will become an

invader of perennial communities. Only one cultivar (Immigrant)

has been released in the United States. Eighty-one forage kochia

plantings (mainly Immigrant) were evaluated to document forage

kochia’s adaptation and spread. Ecological descriptions were taken

for each site and multiple regression analyses were done to determine prediction equations for recruitment outside the original

plantings. Our results indicated that forage kochia is well adapted

to a wide range of semiarid and arid rangelands, but is not an

aggressive spreader. However, it may recruit into playas, slick

spots, and disturbed and/or degraded areas. The fringe of recruitment, defined as the marginal recruitment threshold, ranged from

0 to 100 ft with a mean and median distance of 20 ft. Regression only

explained 22 percent of fringe threshold variation and consisted of

the following factors: medium textured soils, lower elevation, and

age of seeding. Unexplained variation may be due to factors not

determined, such as the disturbed peripheral area surrounding

each planting.

Introduction ____________________

“Immigrant” forage kochia [Kochia prostrata ssp. virescens],

a half-shrub, has been seeded on over 200,000 acres of

rangeland in 10 western states. Many scientists and rangeland managers consider forage kochia a prime candidate for

western range rehabilitation and fire prevention. However,

others are concerned about its potential to invade and

suppress or eliminate native plant populations. Many are

concerned that because forage kochia is an introduced species it may spread vigorously throughout western rangelands. We conclude that these concerns are largely unfounded. This investigation was undertaken to examine

Immigrant forage kochia’s competitive ability, invasiveness

and potential effects on bio-diversity of native and introduced plant communities on semiarid rangelands.

During October 1999, two of the authors (Waldron and

Harrison) participated in a forage kochia germplasm collection trip to Kazakhstan. They evaluated forage kochia’s

compatibility and aggressiveness in its native environment

on 64 sites.

Immigrant forage kochia was released in the United

States in 1984 (Stevens and others 1984). Immigrant is

native to the arid and semiarid regions of Central Eurasia

(Larin 1956; Keller and Bleak 1974; Plummer 1974). The

parental accession (PI314929) of Immigrant, along with

other accessions, was acquired in May 1966 in a search for

plants to suppress halogeton [Halogeton glomeratus) on

droughty and saline sites. Immigrant, the only North American cultivar of the ssp. virescens (green-stem forage kochia)

is a diploid with a chromosome number of 2n = 18 (Pope and

McArthur 1977; Herbel and others 1981).

The first known Immigrant (PI 314929) planting in the

U.S. was made in l968 by Keller and Bleak (1974). Immigrant was jointly released in March l984 by the USDA Forest

Service, USDA Soil Conservation Service, the Utah Division

of Wildlife Resources and the Idaho, Nevada, Oregon, and

Utah Agriculture Experiment Stations.

Forage kochia is a long-lived, semi-evergreen half shrub

that averages 1 to 3 ft high at maturity. Individual plants

may live 10 to 15 years (Balyan 1972). It develops an

extensive fibrous root system with a tap root that may

extend to a depth of 16 ft (Prianshnikov 1976). It does not

tolerate flooding or soil with a water table (Balyan 1972).

Seeds ripen in October and November (Prikhod’ko and

Prikhod’ko 1977), however, freezing temperatures hasten

seed ripening. There are approximately 115,000 pure live

seeds per lb (Stevens and others 1996). Forage kochia seeds

germinate well for 6 to 8 months after harvest. It may

maintain good germinability for up to 3 years if seed is

properly dried to 7 percent or less moisture and stored at 36

to 50 °F (2.2 to 10 °C) (Jorgensen and Davis 1984).

Immigrant is widely adapted and has been successfully

established on a range of soils including fine-to-coarse textured, shallow-to-deep, gravelly-to-stony and saline-to-alkaline and in numerous plant communities from mountain

to desert shrub.

Uses __________________________

Immigrant has been seeded to improve plant community

diversity, esthetics, plant cover, species richness, forage for

domestic livestock and wildlife, fire prevention, and improved soil stability. Specific examples of its use are to

(1) prevent accelerated soil erosion, flooding, and critical
USDA Forest Service Proceedings RMRS-P-21. 2001 211

Forage Kochia: Friend or Foe Waldron, Harrison, Chatterton, and Davenport

area treatment including blowout areas (Stevens and others

1984; Rassmussen and others 1992; Horton, unpublished

data 1998); (2) supply livestock and wildlife forage during

normal and critical periods (Otsyina and others l983; Gade

and Provenza 1986; Kashkarov and Balyan 1989; Bake

1997); (3) provide food and cover for upland game birds,

small mammals, reptiles, and insects (Stevens and others

1985); (4) readily provide ground cover on disturbed areas

(Nemati 1986; Blauer and others 1993); (5) suppress or

eliminate alien invasion of annual weeds like cheatgrass

(Bromus tectorum), halogeton [Hologeton glomeratus], Russian thistle [Salsola pestifer], and medusahead rye [Taeniatherum (Elymus) caput-medusae], (Van Epps and McKell

1983; McArthur and others l990; Stevens and McArthur

1990; Monsen and Turnipseed 1990; Monsen 1994; Gutknecht

1996; Simper, personal communication, NRCS, Cedar City,

UT, 1997; Turnipseed, personal communication, Idaho Fish

and Game, Caldwell, ID, 1998); (6) reclamation of disturbed

mine sites (Howard and others 1976; Frishchknecht and

Ferguson 1984; Clements and others 1997); (7) beautify and

stabilize road sides (Plummer 1970; Blauer and others

1993); (8) stabilize sand dunes (Krylova 1988); (9) increase

species richness and biodiversity and assist in the reestablishment of desired perennials (Blauer and others 1993;

Gutknecht 1996; Clements and others 1997); (10) provide

green strips that suppress or prevent wild fires (Pellant

1990; Monsen 1994; Clements and others 1997); and

(11) extract salts (sodium and chloride) from saline soils

(Larin 1956; Francois 1976).

Competition, Invasiveness, and

Biodiversity ____________________

Expression of a plant’s competitive ability is a function of

environmental and site conditions. Important environmental considerations are geomorphology, slope, aspect, soil

type, climate, salinity, human impacts, seed sources, and

existing or competing vegetation. All plants, both native and

introduced, spread and compete in environments where

they are best adapted and where there is little or no competition by other species for resources (Harrison and others

1996).

Immigrant forage kochia appears to have a competitive

advantage over many other species in the cool shrub steppe

because of its temporal and spatial capacity for water uptake

(Romo and Haferkamp 1987). Under some conditions it can

rapidly deplete soil moisture and become established in the

presence of annual and perennial competitors (Keller and

Bleak 1974; Van Epps and McKell 1983; Stevens and others

1985; Romo and Haferkamp 1987). The competitive advantage of Immigrant on disturbed sites over annuals like

cheatgrass and halogeton is well documented (McArthur

and others 1990; Monsen and Turnipseed 1990).

In its natural range in south-central Eurasia forage kochia

is commonly associated with grasses and Artemisia species

and contributes significantly to plant biodiversity. We concur with others that it generally does not grow in pure stands

in its native habitats in Eurasia (Plummer 1970; McArthur

and others 1974). In the U.S., Immigrant forage kochia

appears to be best adapted within its ecological range when

there is little competition from established perennial species.

The Bureau of Land Management in Idaho found that

Immigrant has spread a few meters in disturbed areas

beyond the original seeded boundaries on several 1986

greenstrip seedings (M. Pellant, BLM, personal communication, Boise, ID, 1998). Several researchers (Blauer and

others 1993; Stevens and others 1985; Pendleton and others

1992; Clements and others 1997; K. Gray, personal communication, Nevada Division of Wildlife, Elko, NV, 1998; M.

Haferkamp, personal communication, USDA-ARS, Miles

City, MT, 1998) have concluded from studies in the big

sagebrush and desert shrub communities that Immigrant is

not highly invasive and does not spread aggressively into

healthy plant communities.

Clements and others (1997), (C. D. Clements, personal

communication, USDA-ARS, Reno, NV, 1999) states, “In the

sagebrush/bunch grass region of the Great Basin, forage

kochia does not appear to be invasive.” They found little to

no movement outside of 17 established seedings ranging

from 2 to 17 years old. They concluded that “areas must be

reduced to bare soil before it successfully invades.” Stevens

and others (1984) reported that Immigrant out competes

many annuals, fills in the inter spaces between perennials,

and establishes well when co-seeded with other perennials.

They noted its recruitment into a black greasewood

[Sarcobatus vermiculatus]-shadscale [Atriplex confertifolia]-

halogeton community, and into introduced plant communities of intermediate wheatgrass [Thinopyrum intermedium],

crested wheatgrass [Agropyron cristatum], cheatgrass, and

medusahead rye. A. DeBolt (personal communication, USDI

BLM, Boise, ID, 1998) indicated that pepper plants (Lepidium

davisii and papillienum) species may suffer due to

Immigrant’s tendency to colonize on saline and alkaline

playas. Blauer and others (1993) noted that in higher precipitation zones, Immigrant does not compete well in a

closed herbaceous plant community.

In 1998, Clements (personal communication, 1999) found

in Immigrant seedings that the density of cheatgrass declined and that native species numbers were seven times

greater than in adjacent unburned stands. Clements and

others (1997) concluded that native plants will become

established in Immigrant seedings if fires are infrequent.

They reported the spread of Wyoming big sagebrush,

thickspike wheatgrass [Elymus lanceolatus], native bunch

grasses and forbs was common in the fourth growing season

of a stand of Immigrant, which had first suppressed

cheatgrass.

Materials and Methods ___________

This study was designed to determine planting success,

biodiversity, spread, and competition of Immigrant forage

kochia on semiarid western rangelands. In our attempt to

assess the responses of Immigrant to the varied rangeland

conditions into which it has been seeded in the Intermountain West we: (1) sent questionnaires to personnel at state

and national resource agencies and researchers at universities and other institutions who were, or had been, involved

with forage kochia research; (2) visited representative

seedings and/or transplantings throughout the West that

were old enough to give some indication of long term responses. We received over 151 questionnaire responses
212 USDA Forest Service Proceedings RMRS-P-21. 2001

Waldron, Harrison, Chatterton, and Davenport Forage Kochia: Friend or Foe

describing forage kochia plantings. Information from the

questionnaires and published reports was used to determine

which plantings should be visited for further evaluation.

Onsite assessments were made, where possible, to all

known Immigrant plantings that were unique or that were

10 years or older. More than 90 planting sites were visited

and data was collected from 81 sites.

Because of the large number of field sites, the line-intercept method was used to evaluate Immigrant spread and

percent composition. Transects were randomly located in

plantings and a 100-foot tape was laid parallel to the original

planting. Individual species, litter, bare ground and rocks

were recorded. Percent plant composition was calculated for

each species as the percentage of the total vegetation comprised by that species. A visual reconnaissance survey was

made to assess the spread of forage kochia into fringe areas

adjacent to the original planting, and the maximum distance

from the seeding’s edge where a single Immigrant plant had

become established was recorded. The fringe distance was

defined as the visual marginal or peripheral threshold of

Immigrant encroachment from the original seeded boundary. In many instances, recruitment away from the seeding

occurred in a pattern of fingers or pockets. At such sites a

transect was taken within the finger or pocket at the visually

observed threshold area of recruitment. If spread appeared

to be mainly uniform around the planting then random

transects were taken at the visually observed fringe. If no

spread was observed then the fringe distance was recorded

as zero. It should be noted the evaluation areas for each site

were randomly selected and may not completely represent

the entire planted area. Planting boundaries were shown to

us by field personnel. Recruitment data were not taken

when original seeding boundaries were unknown.

Statistical Analysis ______________

Independent variables were treated as continuous (for

example, elevation, precipitation, and so forth), interval

categorical (for example, results = poor, fair, good, or excellent), or dichotomous categorical (yes or no) for correlation

and regression analysis.

Questionnaire

Information obtained from the questionnaires was subjected to correlation analysis using SAS software (1989) to

search for significant (P <0.10) associations between independent environmental factors and the perceived degree of

success in establishment and recruitment of forage kochia

outside the planting area.

Onsite Assessment

All possible correlation coefficients (r) (SAS 1989) were

calculated between dependent variables (maximum distance to a single plant, fringe of recruitment, percent Immigrant composition at the fringe, percent Immigrant

composition inside original seeding) and independent environmental variables as determined by site visits or from the

questionnaires and published literature.

Stepwise multiple regression procedures (SAS 1989) were

performed on independent variables to identify the best

multiple regression model for the dependent variables. Independent variables that failed to maintain significance were

eliminated. Multiple regression was repeated using the MAXR

option of SAS (1989) to determine the maximum R2 obtainable using the independent variables estimated. The resulting R2 from these multiple regression models is indicative of

the proportion of total variation in forage kochia spread and

composition explained by the independent variables. It is

possible that interactions between independent factors may

have significantly increased the predictive power of the

regression models, but because of degree-of-freedom limitations and complexity of interpretation, we did not test

interactions. Planting-method variables were not included

in the stepwise regression procedures because of the limited

number of sites for which that information was known.

Results ________________________

Adaptation and Stand Composition Within

Orginal Seeding

Percent composition of Immigrant within original seedings

ranged from 2 to 91 percent with an average of 50 percent

and median of 53 percent . Factors favorably associated with

higher Immigrant composition included seeding date, medium textured soils, Immigrant planted with no other species, prepared or disturbed seedbed, successful initial establishment, and predominantly annual competition (table 1).

Stepwise regression analysis resulted in an R2 of 44 percent

(table 1). Including all independent variables in the regression model resulted in a maximum R2 of 58 percent . Unexplained variation may be due to factors not determined such

as quality of seed, seeding rate and date, or interactions

among environmental variables.

Fringe of Recruitment

Fringe distance, or marginal or peripheral recruitment

threshold, ranged from 0 to 100 ft. The mean and median

were both 20 ft. These small values for the mean and median

strongly suggest that in most environments, Immigrant is

not an aggressive competitor with native or established

vegetation. The best regression model, consisting of medium

soil texture, elevation, and date of seeding, only explained 22

percent of variation in recruitment fringe distance (table 1).

Even though date of planting was included in the multiple

regression model, the plot of planting date versus fringe

suggests a very weak association between the two (fig. 1).

The maximum R2 achievable using all estimated variables

still only explained 48 percent of the variation. Unexplained

variation may be due to factors that were not determined

such as variations in annual precipitation during the life of

the seeding.
USDA Forest Service Proceedings RMRS-P-21. 2001 213

Forage Kochia: Friend or Foe Waldron, Harrison, Chatterton, and Davenport

Table 1—Correlation coefficients and associated P-value, P-value from stepwise multiple regression, and

R2

 for multiple regression model for ecosite variables associated (P ≤0.10) with percent forage

kochia composition within seeding and fringe of forage recruitment outside of planting (58 sites

included in analysis).

Variable r P-value (individual) P-value (mult. reg.)

Forage kochia percent within seeding

Monoculture seeding 0.43 0.001 0.001

Disturbed seedbed 0.41 0.001 0.020

Perennial competition –0.42 0.002 .

Medium textured soils 0.29 0.026 .

Annual competition 0.29 0.034 .

Coarse textured soils –0.27 0.038 .

Elevation –0.25 0.057 0.018

Fire before planting –0.28 0.058 .

Seeding date 0.24 0.065 .

Precipitation –0.24 0.068 .

Successful establishment 0.23 0.077 .

Pinyon-juniper ecosystem –0.23 0.087 .

Basin big sagebrush ecosystem –0.23 0.087 0.010

R2

 = 44 percent

Fringe of forage kochia recruitment

Medium textured soils 0.30 0.021 0.018

Salt desert shrub ecosystem 0.24 0.067 .

Elevation –0.22 0.090 0.4

Fire before planting –0.22 0.098 .

Pinyon-juniper ecosystem –0.21 0.100 .

Age of planting . . 0.063

R2 = 22 percent

Maximum Distance From Seeding to a

Single Plant

Reconnaissance surveys of the perimeters surrounding

62 Immigrant plantings found individual plants at 0 to 1,265

ft from the seeding boundary. The mean and median distances were 93 ft and 50 ft, respectively. These numbers

indicate that although individual plants were found at a

considerable distance from the boundary at a few sites, the

furthest single immigrant plant at half the sites was 50 feet

or less from the original planting. The best multiple regression model only explained 6 percent of the variation among

sites, further indicating the evaluated environmental variables could not be used to predict this measure of spread. No

ecosite variables were significantly correlated with maximum distance to single forage kochia plants.

Immigrant Forage Kochia Composition

at Recruitment Fringe

On average Immigrant comprised only 6 percent of the

vegetation at the defined recruitment fringe (range was 0 to

26 percent ). The median value for immigrant composition at

the fringe was 4 percent . The most significant correlation

found was with age of planting.

From the low R2 values for these measures of recruitment

it is obvious that unknown factors are important in determining the extent of forage kochia recruitment. Our observations suggest that the extent of severe soil disturbance

around the planting may have a large impact on the

recruitment.

Discussion and Summary

The complete report of this study can be found at (Harrison

and others 2000). Our findings are in agreement with and

generally confirm reports in literature. Immigrant will naturally recruit, like the majority of plants, mainly in disturbed

soil or in areas lacking vegetation, especially perennial

vegetation, both within and outside its seeding area. The

major elements that influence the distance and amount a

species will spread are its ecological adaptation, amount of

soil disturbance, and plant competition from both annuals

and perennials. Immigrant kochia has a broad diverse

adaptability and therefore propagates itself in several western rangeland plant communities.

Sites with high annual precipitation supported less kochia

spread than those with lower annual precipitation. High

precipitation zones may have more closed plant communities and less open spaces for kochia establishment than

lower rainfall areas. Immigrant establishes well in course,

medium, and fine textured soils including sandy, gravely,

stony, clay, silt, and loam soils.

Long-term research is needed to determine Immigrant’s

competitive interaction with perennials in the Wyoming big

sagebrush, desert shrub (black sagebrush and shadescale),

and salt desert shrub sites. Our observations suggest that

over time native perennials, such as shadscale, winterfat,

Wyoming big sagebrush, thickspike wheatgrass and western wheatgrass [Pascopyrum Smithi] may reestablish themselves in stands of Immigrant forage kochia. In many

instances, resource mangers are currently faced with the

persistence of alien annuals such as cheatgrass and
214 USDA Forest Service Proceedings RMRS-P-21. 2001

Waldron, Harrison, Chatterton, and Davenport Forage Kochia: Friend or Foe

medusahead rye that result in increased frequency of wildfires and degradation of the resource base through soil

erosion. The establishment of Immigrant forage kochia

helps protect these environmental resources and allows

native perennial communities to become re-established. On

many evaluated sites, biodiversity has been improved by the

presence of Immigrant. Clearly, Immigrant can be established in a wide range of areas and environmental conditions. It successfully competes with annuals, such as

cheatgrass, halogeton, Medusahead rye, and tumble mustard (Sisymbrium altissimum). Although Immigrant may

spread into disturbed and bare areas, especially on sites

with minimal productivity, low elevation, low precipitation,

and saline/alkaline soils, including playas and slick spots,

we found little evidence that Immigrant is an aggressive

spreader in established perennial plant communities.

Our conclusions from evaluations in Kazakhstan and

discussions with Russian and Kazakhstan scientists concerning the spread of forage kochia into native perennial

plant communities are in full agreement with our assessments of its adaptation and aggressiveness in the U.S.A.

Depending on the site and associated species, native perennial plant communities in Kazakhstan contained from 1 to

20 percent forage kochia. However, in disturbed areas along

roadways, abandoned fields, and farmsteads, forage kochia

made up from 15 to 60 percent of the plant community.

Forage kochia was never observed to be the dominant

species in the major plant communities compromised of

sagebrush, saltbush, winterfat, crested and siberian wheatgrasses, and needlegrass. Nowhere did we observe sites

where forage kochia had invaded from disturbed sites into

adjacent perennial plant communities on the Kazakhstan

steppes.

References _____________________

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USDA Forest Service Proceedings RMRS-P-21. 2001 215

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216 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Barbara A. Wachocki is Associate Professor of Botany, Botany Department, and Mohammad Sondossi is Professor of Microbiology, Microbiology

Department, Weber State University, Ogden, UT 84408. E. Durant McArthur

is Project Leader and Supervisory Research Geneticist, and Stewart C.

Sanderson is Research Geneticist, U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station, Shrub Sciences Laboratory,

Provo, UT 84606. Bruce L. Webb is Director of the Plant and Soil Laboratory,

Department of Agronomy and Horticulture, Brigham Young University,

Provo, UT 84602.

Abstract—The objectives of this study were to determine

tebuthiuron’s (1) effectiveness at low application rates in thinning

dense, high elevation stands of mountain big sagebrush, (2) impact

on understory herbaceous plants and soil microflora, and (3) movement and stability in soil. Four study sites were established in the

Fish Lake National Forest and adjacent Bureau of Land Management holdings. Tebuthiuron pellets were applied at one site in 1994,

a second site in 1995, and two sites in 1996 at rates ranging from 0.2

to 0.7 pounds of active ingredient (AI) per acre (0.18 to 0.63 kg AI per

ha). Data from the two sites treated in 1996 show that sagebrush

canopy cover was reduced in annual increments from pretreatment

levels of about 23 percent to11 percent (0.3 AI treatment), 6 percent

(0.5 AI), and 4 percent (0.7 AI) by 1999 (control plots were 26 percent

by 1999). Understory vegetation increased slightly or had no change

over time depending on treatment and climatic factors. Tebuthiuron

treatments at these rates did not have long-term adverse effects on

soil microflora. Tebuthiuron was mobile and its concentration

remained twice as high in the zero to 15 cm soil samples as compared

to deeper soil samples (>15 to 30 cm). Overall, tebuthiuron levels

dropped about six fold from the second to third year after application

(to 0.1 ppm). The preliminary conclusion is that tebuthiuron applied

at these low concentrations can maintain mountain big sagebrush

cover at meaningful levels without damage to the understory and

soil micoflora.

Introduction ____________________

Tebuthiuron, N[5-(1,1-dimethylethyl)-1,3,4-thidiazol-2-

yl]-N-N’-dimethylurea, is an herbicide that is used to thin

dense stands of woody plants in rangelands in order to

increase access to forage plants in the understory. It has

Impact of Tebuthiuron on Biodiversity of

High Elevation Mountain Big Sagebrush

Communities

Barbara A. Wachocki

Mohammad Sondossi

Stewart C. Sanderson

Bruce L. Webb

E. Durant McArthur

been used in many studies to control big sagebrush, Artemisia spp., (Britton and Sneva 1984; McDaniel and Balliette

1986; Whitson and Alley 1984). Tebuthiuron is applied to the

soil surface as pellets and thus its movement through soil

can be affected by soil type and moisture (Johnsen and

Morton 1989). Studies have shown that tebuthiuron is

highly mobile in soil and levels typically decrease rapidly in

1 to 4 years after treatment (Emmerich and others 1984;

Johnsen and Morton 1989). Despite this initial rapid decrease, in one study Johnsen and Morton (1989) have shown

that concentrations were detectable throughout the study

and actually began to steadily increase 9 to 11 years after

treatment (11 year study). It has been suggested that this

may be due to slow release from soil particles or from slowly

decaying litter (Garcia and Lee 1979). Long-term effects of

residual tebuthiuron may be of particular importance in arid

soils.

It is therefore important to determine if low doses of the

herbicide can still be effective in thinning woody species

while minimizing any possible detrimental effects on the

community as a whole. This study examined the impact of

tebuthiuron in low concentrations (0.18 to 0.63 kg AI per ha)

on high elevation mountain big sagebrush (Artemisia tridentata ssp. vaseyana) communities. In addition to its effectiveness against the target species, this study sought to

determine if tebuthiuron has an impact on understory plants

or on soil microflora.

The functional composition and diversity of plant communities have been shown to be the principal factors controlling

productivity (Hooper and Vitousek 1997; Tilman and others

1997). These findings suggest that management practices

affecting plant diversity and composition can have a profound effect on ecosystem processes. Although compounds

such as herbicides and insecticides are, in general, less

detrimental to microbial activities, some soil microbial processes and properties may be affected (Hicks and others

1990; Nemes-Kosa and Cserhati 1995). This possible impact

on soil microbial communities should be evaluated in view of

their role in sustaining the global cycling of matter and their

varied functions in supporting plant growth. Assessment of

the impact of changes in plant communities on soil community structure is difficult because of the highly diverse

nature of microbial communities in soil. This may be facilitated by investigation of specific groups of microorganisms

or specific activities. Microorganisms involved in the nitrogen cycle are of particular concern since nitrogen is usually
USDA Forest Service Proceedings RMRS-P-21. 2001 217

Impact of Tebuthiuron on Biodiversity of High Elevation Mountain Big Sagebrush Communities Wachocki, Sondossi, Sanderson, Webb, and McArthur

the limiting nutrient in soils and the rate of microbial

activity is limited in arid ecosystems. Due to the limitations

in scope and budget, efforts were concentrated on limited

areas and methodologies. Hence, this study focused on

determining the impact of tebuthiuron treatment on total

heterotrophic microbial populations and aspects of nitrogen

cycling.

Species abundance and diversity measurements are sensitive indicators of environmental conditions. However, the

conventional methodologies investigating diversity of microbial communities have significant shortcomings. These

include the time and resources required to quantify and

identify microbial species of many different groups and

extensive analysis of numerous samples from different treatments. Furthermore, a significant bias is invariably introduced by the selective cultivation, analysis, and interpretation of results. We acknowledge these shortcomings in this

report.

The objectives of this study were (1) to evaluate the

effectiveness of low application rates of tebuthiuron in

thinning dense, high elevation stands of mountain big

sagebrush, (2) to evaluate the impact of tebuthiuron on

understory herbaceous plants and soil heterotrophic bacteria and fungi, ammonium oxidizing microflora, nitrifying/

nitrate reducing (combined assimilatory and dissimilatory

processes) microflora, photosynthetic microflora, and mycorrhizal associations, and (3) to examine the movement and

stability of tebuthiuron in the soil.

Methods _______________________

Study Sites

Four study sites were established in the Fish Lake National Forest and adjacent Bureau of Land Management

holdings: three were on the Monroe Mountain portion of the

Sevier Plateau, designated as the Plateau, Big Flat and

Burnt Flat treatment sites. The fourth site was on the

nearby Fish Lake Plateau and is referred to as the Fish Lake

treatment site. The elevations of the sites are: Plateau, 8,125 ft

(2,508 m); Fish Lake, 8,800 ft (2,716 m); Burnt Flat, 9,300 ft

(2,870 m); and Big Flat, 9,400 ft (2,901 m). All sites were

dominated by mountain big sagebrush. Soils were characterized as loams with 40 to 48 percent sand, 20.56 to 26.56

percent clay, and 29.16 to 33.44 percent silt in all but the

upper depths (zero to 15 cm) at Plateau, which was a clay

loam (29.56 percent clay and 26.42 to 28.16 percent silt). Soil

pH ranged from 5.9 to 6.6. Upper soils typically had more

organic matter than did corresponding deeper soil (>15 to

30 cm). Overall percentages of soil organic matter are:

Plateau, 2.34 to 3.88 percent; Fish Lake, 3.57 to 9.36 percent;

Big Flat, 4.39 to 5.32 percent; and Burnt Flat, 9.46 to 10.70

percent.

Tebuthiuron Application

Study plots measuring 50 x 100 ft (15.24 x 30.48 m) were

established in a random manner and tebuthiuron was applied as pellets in the following concentrations and times at

the four sites: Plateau site, 0.0, 0.3, 0.5, and 0.7 pounds active

ingredient (AI) per acre (0.0, 0.27, 0.45, and 0.63 kg AI per ha)

applied Sept. 29, 1994; Fish Lake site: 0.0, 0.2, 0.4, and 0.6

pounds AI per acre (0.0, 0.18, 0.36, and 0.54 kg AI per ha)

applied Sept.13, 1995; Big Flat site 0.0, 0.3, 0.5, and 0.7

pounds AI per acre (0.0, 0.27, 0.45, and 0.63 kg AI per ha)

applied July17, 1996; and Burnt Flat site 0.0, 0.3, and 0.5

pounds AI per acre (0.0, 0.27, and 0.45 kg AI per ha) applied

July17, 1996. Big Flat and Burnt Flat sites also included

replicate plots.

Vegetation Study

Plant ecological data were collected in the summers prior

to soil sampling. In 1996, vegetation surveys were conducted

before tebuthiuron was applied to the Big Flat and Burnt

Flat treatment sites. Vegetation data were collected over a

4-year period from 1996 to 1999.

Control and treatment plots (about 0.4 ha each) were set

up in areas of level terrain and homogeneous vegetation and

soil. Within each plot a circular 0.01 ha subplot was established in a random manner and centered on a steel rebar

post. Subplot perimeters were at least two meters from the

plot boundary. Data collected in the subplots included vascular plant species present and percent cover partitioned

among shrubs, grasses, forbs, bare soil, liter, rock (>2 cm),

and cryptogams (Daubenmire 1959; McArthur and Sanderson

1992, 1995). Density of plant species was determined from

4 m2 quadrats located 1 m in each cardinal direction from

the center of the circular subplots. Sagebrush cover was

monitored along two 45 m diagonal line transects in each

treatment and control plot. Means separations of data were

performed using Proc Means procedures of the SAS statistical package (SAS 1989).

Soil Sampling

Soil sampling was done during site visits at the four sites

in August 1996, 1997 and 1998. In 1996, soil samples were

taken at two depths (0 to 15 cm and >15 to 30 cm) at the

base of two selected healthy looking plants (healthy) in the

control plots, and one healthy, two slightly unhealthy looking plants (medium affected), and one unhealthy looking

plant (affected) in each of the treated plots at the Fish Lake

and Plateau sites. The plants were tagged and samples were

taken at the base of the same plants in subsequent years. In

addition, pooled (composite) samples from each plot were

taken each year. In 1996 only composite samples were taken

at the Big Flat and Burnt Flat sites. In the subsequent 2 years,

1997 and 1998, a full sampling approach (healthy, medium

affected, affected and composite) was taken at all treatment

sites.

Two to four pounds of soil were collected per sample and

put into plastic airtight bags. Each sample was then mixed

thoroughly and split into two separate labeled bags and

transported on ice to the laboratory. One set was used for soil

chemical analysis and the other for microbial analysis. Soil

samples were kept refrigerated until tests were conducted.

Tebuthiuron and Soil Analysis

Tebuthiuron and its metabolites were extracted from soil

samples with acidified methanol. It was quantified using a
218 USDA Forest Service Proceedings RMRS-P-21. 2001

Wachocki, Sondossi, Sanderson, Webb, and McArthur Impact of Tebuthiuron on Biodiversity of High Elevation Mountain Big Sagebrush Communities

Waters HPLC (Loh and others 1980). Soil classification

(texture class) was made based on percent sand, clay, and

silt. In addition, percent organic matter, pH, and electrical

conductivity were determined.

Microbial Analysis of Soil

Total Heterotrophic Bacteria and Mold Counts—

Serial dilutions of soil samples were made and surface

plated on Trypticase Soy Agar (TSA) and Sabouraud Dextrose Agar (SAB). Plates were incubated at 30 °C for 72

hours. Total bacterial and fungal counts were made. The

plates were reincubated and checked again after 5 days to

observe slow colony forming organisms. The counts were

amended as required.

Estimation of Nitrifying and Nitrate-Reducing Microbial Populations—Soil samples were taken from the

base of healthy plants in control plots, and healthy and

affected plants in the highest treatment plot at each site.

The MPN method described by Alexander (1982) was used

and an estimation of nitrifying populations was made using

the method described by Schmidt and Belser (1982). A total

of 25 tubes of each medium, ammonium oxidizer and nitrite

oxidizer media, for each soil sample were used. Samples

were incubated at room temperature with light.

The presence of ammonium was determined in incubated

samples using Nessler’s reagent, nitrite and nitrate were

detected using modified Griess-Ilosvay reagents, and diphenylamine, respectively (Schmidt and Belser 1982). A sample

was considered positive for ammonium oxidation if nitrite

and/or nitrate were detected after incubation in ammonium

medium. A sample was considered positive for nitrite oxidation when all nitrite was exhausted from the medium or

nitrate was detected in the total absence of nitrite in the

nitrite medium. Complete oxidation to nitrate and subsequent removal of nitrate (assimilatory reduction by incorporation into cell material and/or dissimilatory reduction to N2

gas) could be concluded by the absence of nitrite and nitrate

in nitrite medium.

Estimation of Photosynthetic Microbial Populations

(Algae and Cyanobacteria)—During examination of plates

and MPN tubes in 1996 and 1997, green colonies with mixed

bacterial and photosynthetic microorganisms were seen on

some plates and green-pigmented growth was observed in

several MPN tubes. The most vigorous growth was found in

nitrite medium when incubated in light. This provided an

opportunity to compare the photosynthetic microbial communities in samples from control and the highest treated

plots at each site using the MPN method. This was done

using samples taken in 1998.

Mycorrhizal Association—In the first year (1996) root

samples of more than 20 plant species from control plots at

the Fish Lake and replicate Big Flat sites were collected and

examined for the presence of mycorrhizal associations. Each

root sample was washed thoroughly with tap water through

a 1 mm sieve, retaining the roots on top of the sieve. The

washed roots were preserved in FAA (5 percent Formalin, 5

percent Acetic acid, 40 percent Ethanol, 50 percent H2O)

until needed.

Ectomycorrhizae: Each root sample was spread out in a

petri dish with enough FAA to keep roots immersed. Small

pieces of root tips were stained in lacto-phenol-cotton blue,

transferred to clear lacto-phenol, mounted on a slide in clear

lacto-phenol under a coverslip, and examined under a microscope for the presence of ectomycorrhizal associations.

Endomycorrhizae and Vesicular-Arbuscular Mycorrhizae

(VAM): Small pieces of root tip were placed in perforated

microfuge tubes. The roots were placed in a beaker containing 10 percent KOH and autoclaved at 121 °C for 10 minutes.

Roots were then rinsed in tap water, bleached in 30 percent

hydrogen peroxide for 10 minutes, and rinsed with tap water

three times. The roots were covered in 1 percent HCl for 3 to

4 minutes without rinsing and stained with Trypan Blue for

20 minutes in a hot water bath (90 °C). Roots were then

placed in 40 percent glycerin and examined microscopically.

Photomicrographs were taken for documentation.

In 1997 and 1998, the above procedure was used to

examine the mycorrhizal associations in selected plant species in control and the highest treatment plots at all four

sites.

Results ________________________

Soil Concentrations of Tebuthiuron

Soil chemical analyses from the Plateau and Fish Lake

sites were pooled, as were those from the Big Flat and Burnt

Flat sites (table 1). Tebuthiuron was detected up to 100 ft

(30.48 m) from the areas of application after the first year.

Tebuthiuron concentrations remained significantly higher

(at least double) in the upper 15 cm of soil as compared with

deeper soil samples throughout the duration of the study.

The final measured tebuthiuron concentrations (2 years

after application) were significantly (80 to 83 percent) less

than those measured in the previous year. There was no

significant difference in tebuthiuron concentrations among

treatments.

Vegetation Study

Plant community sampling spanned a 4-year period (1996

to 1999). Results from the Big Flat and Burnt Flat sites are

presented. Similar trends were seen at the other sites. The

percent cover of mountain big sagebrush (table 2) was not

Table 1—Tebuthiuron concentrations (ppm); treatment is in pounds of

active ingredient per acre.

Soil depth

Soil depth >15 to

 Location Time frame 0 to 15 cm 30 cm Significancea

Plateau and

 Fish Lake All years 0.40 0.16 NS

1997–1998 0.50 0.09 *

Treatment NS

Big and

 Burnt Flat All years 0.54 0.27 *

1997–1998 0.69 0.11 *

Treatment 0 0.3 0.5 0.7

0.14 0.38 0.38 0.33 NS

a

* = P < 0.05, NS = not significantly different.
USDA Forest Service Proceedings RMRS-P-21. 2001 219

Impact of Tebuthiuron on Biodiversity of High Elevation Mountain Big Sagebrush Communities Wachocki, Sondossi, Sanderson, Webb, and McArthur

significantly different among plots prior to herbicide application. In each subsequent year after tebuthiuron application sagebrush cover decreased with increasing tebuthiuron

concentration, while remaining almost constant in control

plots. Treated plots had significantly less sagebrush cover

than did control plots.

The density of perennial grasses (table 3) was not significantly different with increased tebuthiuron concentrations.

Overall, the density was highest in 1998, but there was no

significant difference between years. The density of native

perennial grasses also peaked in 1998, but again there was

no significant difference among years (McArthur and

Sanderson, data on file at Shrub Sciences Laboratory).

There were, however, significantly fewer native perennial

grasses in the highest herbicide treatment plots as compared with control plots. The densities of native perennial

forbs and native annuals were not significantly different

among treatments (McArthur and Sanderson, data on file at

Shrub Sciences Laboratory). The density of native perennial

forbs increased significantly while the density of native

annuals decreased significantly in later years (1998 an

1999) as compared with earlier years.

Soil Microbial Study

Results from all four sites were similar. Total soil heterotrophic bacterial counts ranged from 106 to 107 as seen on

TSA with the exception of 1998 (zero to 15 cm) at Big Flat,

where all plots produced 104 to 105 bacteria (data not

shown). Total soil mold counts ranged from 104 to 106

. Data

from Fish Lake will be presented and are representative of

the other sites. Total heterotrophic bacterial counts (fig. 1)

and total mold counts (fig. 2) did not differ significantly

among treatments, years, or soil depth.

There was essentially no significant difference in the MPN

of nitrite oxidizers (fig. 3) or in the MPN of nitrate reducers

(fig. 4) isolated from soil near plants in control and heavily

treated plots or in samples collected in different years. There

were slightly more nitrite oxidizers and nitrate reducers in

the soil samples from the base of healthy plants in the

treated plot as compared with that of affected plants in the

same plot and controls. There was virtually no difference in

the detected MPN of ammonium oxidizers among treatments or between healthy and affected plants (fig. 5). The

detected MPN of ammonium oxidizers varied slightly between years, but the results were very consistent among

treatments and plants.

Mycorrhizal Study

There were essentially no differences found in the quantity or type of mycorrhizal associations found on root samples

among control and treated plots or in different years (data

not shown). Virtually all root samples examined had

endomycorrhizal associations.

Photosynthetic Soil Microflora

In the last year of the study (1998), the MPN, based on

green-pigmented growth in nitrite tubes, was used to compare and quantify photosynthetic soil populations. The MPN

of control and the highest treated plots from all sites showed

no persistent effect among treated and untreated plots on

photosynthetic microbial populations.

Discussion _____________________

Tebuthiuron was shown to be mobile in the soils in this

study. This concurs with a previous study by Whisenant and

Clary (1987), which found that tebuthiuron is dispersed over

greater lateral distances in loam soils of low organic content

(such as those in this study) than those of high organic

content. The results of this study are consistent with several

other reports (Bovey and others 1978; Garcia and Gontarek

1975; Johnsen and Morton 1989; Whisenant and Clary

1987) showing that tebuthiuron is found in higher concentrations in upper soil levels. Emmerich and others (1984)

found that tebuthiuron applied at 0.84 kg AI per ha decreased by 62 percent after 21 months. The results of the

present work showed a similar trend, an 80 to 83 percent

decrease 2 years after treatment. Johnsen and Morton

(1989) showed that tebuthiuron can persist in the soil for

many years (particularly in a semiarid environment) and

exert herbicidal activity on vegetation for several years, it

is therefore necessary to determine minimum dosages

required to achieve the desired effects while avoiding

over-dosing to prevent undesirable prolonged effects on an

ecosystem.

The present study showed that low levels of tebuthiuron

were extremely effective in decreasing the cover of mountain

big sagebrush for at least 3 years. Overall, sagebrush cover

Table 2—Percent cover of mountain big sagebrush after tebuthiuron

treatment at Big Flat and Burnt Flat treatment sites.

Yearb

Treatment levela 1996 1997 1998 1999

0 22.9 A 24.6 A 24.9 A 25.9 A

0.3 23.3 A 15.2 B 12.3 B 11.0 B

0.5 24.9 A 13.1 B 7.2 B 6.3 B

0.7 19.2 A 7.0 B 5.1 B 4.3 B

a

Active ingredient in pounds per acre.

b

Different letters in rows and columns indicate significantly different mean

values, P < 0.05.

Table 3—Density of perennial grasses after tebuthiuron treatment

at Big Flat and Burnt Flat treatment sites.

Yearb

Treatment levela 1996 1997 1998 1999

0 180 B 287 AB 328 A 308 A

0.3 147 B 210 A 235 A 228 A

0.5 163 A 208 A 228 A 206 A

0.7 74 A 136 A 139 A 131 A

Year 155 A 225 A 251 A 236 A

a

Active ingredient in pounds per acre.

bDifferent letters in rows indicate significantly different mean values,

P < 0.05.
220 USDA Forest Service Proceedings RMRS-P-21. 2001

Wachocki, Sondossi, Sanderson, Webb, and McArthur Impact of Tebuthiuron on Biodiversity of High Elevation Mountain Big Sagebrush Communities

1E0

1E1

1E2

1E3

1E4

1E5

1E6

1E7

1E8

Control 0.2 0.4 0.6

Pounds active ingredient/acre

Log # Organisms

1996 (0-15 cm) 1997 (0-15 cm) 1998 (0-15 cm) 1996 (15-30 cm) 1997 (15-30 cm) 1998 (15-30 cm)

1E0

1E1

1E2

1E3

1E4

1E5

1E6

Control 0.2 0.4 0.6

Pounds of active ingredient/acre

Log # Organisms

1996 (0-15 cm) 1997 (0-15 cm) 1998 (0-15 cm) 1996 (15-30 cm) 1997 (15-30 cm) 1998 (15-30 cm)

Figure 1—Total soil heterotrophic bacterial counts after tebuthiuron treatment at the Fish Lake treatment site. Data from

soil near healthy, medium affected, and affected plants were similar and are pooled.

Figure 2—Total soil mold counts after tebuthiuron treatment at the Fish Lake treatment site. Data from soil near

healthy, medium affected, and affected plants were similar and are pooled.
USDA Forest Service Proceedings RMRS-P-21. 2001 221

Impact of Tebuthiuron on Biodiversity of High Elevation Mountain Big Sagebrush Communities Wachocki, Sondossi, Sanderson, Webb, and McArthur

1E0

1E1

1E2

1E3

1E4

1E5

Control 0.6 Healthy 0.6 Affected

Log of MPN/gram

1996 (0-15 cm) 1997 (0-15 cm) 1998 (0-15 cm) 1996 (15-30 cm) 1997 (15-30 cm) 1998 (15-30 cm)

1E0

1E1

1E2

1E3

1E4

1E5

Control 0.6 Healthy 0.6 Affected

Log of MPN/gram

1996 (0-15 cm) 1997 (0-15 cm) 1998 (0-15 cm) 1996 (15-30 cm) 1997 (15-30 cm) 1998 (15-30 cm)

Figure 3—Most Probable Number (MPN) of nitrite oxidizers after tebuthiuron treatment at the Fish Lake

treatment site. Soil samples were taken from the base of healthy control plants and healthy and affected plants

in the highest treatment plot (0.6 pounds active ingredient per acre).

Figure 4—Most Probable Number (MPN) of nitrate reducers after tebuthiuron treatment at the Fish Lake

treatment site. Soil samples were taken from the base of healthy control plants and healthy and affected

plants in the highest treatment plot (0.6 pounds active ingredient per acre).
222 USDA Forest Service Proceedings RMRS-P-21. 2001

Wachocki, Sondossi, Sanderson, Webb, and McArthur Impact of Tebuthiuron on Biodiversity of High Elevation Mountain Big Sagebrush Communities

was less in treated plots as compared with controls. There

was a trend, although not significant, for sagebrush cover to

decrease with increased herbicide concentration. Considering the long-term study mentioned above it could therefore

be a concern that tebuthiuron may continue to exert its

effects for a long time and may decrease target species to

lower levels than necessary or desired. The study also

showed that concentrations above the lowest level used here

may not be necessary and concentrations lower than those

used in this study may actually achieve the desirable results.

The densities of perennial grasses and native perennial

grasses were greater after treatment, though not significantly so. The concentration of tebuthiuron had no significant effect on these groups except that there were significantly fewer native perennial grasses in the highest treatment

level. In the second and third years after treatment there

were significantly more perennial forbs and significantly

fewer native annuals than in earlier years. The level of

tebuthiuron did not have any significant effect on these

groups. It is probable that the annuals declined as competition with perennial understory plants increased. These

results suggest that tebuthiuron concentrations as low as

0.27 kg AI per ha could be effective in reducing big sagebrush

cover, while having very little adverse effects on herbaceous

plants in the community.

It is widely accepted that analysis of changes in the

composition of a community can be used to characterize its

response to stress. In order to observe effects by quantifying

changes in microbial biomass or in the general metabolic

activities of microbial communities, a variety of tests have

been recommended (Gerber and others 1991) and employed.

Some may argue that species abundance and diversity are

the most sensitive indicators of environmental conditions

and that a community’s composition and diversity are most

significantly represented by the nucleic acid profiles of

organisms present in the soil (Engelen and others 1998). We

acknowledge that comprehensive studies employing the

most advanced and proven methodologies are required to

derive the most meaningful and accurate conclusions. However, in the absence of studies on the impact of tebuthiuron

on microbial populations and activities, and a limited scope

and budget, results generated from the present study are a

step in the right direction.

Our work indicates that neither heterotrophic microbial

populations (bacteria and mold) nor nitrifying activities at

these sites were affected by tebuthiuron. This is in agreement with the general view that herbicides are less detrimental to microbial activity and, under certain conditions,

may even stimulate certain activities (Hicks and others

1990).

1E0

1E1

1E2

1E3

1E4

Control 0.6 Healthy 0.6 Affected

1996 (0-15 cm) 1997 (0-15 cm) 1998 (0-15 cm) 1996 (15-30 cm) 1997 (15-30 cm) 1998 (15-30 cm)

Log of MPN/gram

Figure 5—Most Probable Number (MPN) of ammonium oxidizers after tebuthiuron treatment at

the Fish Lake treatment site. Soil samples were taken from the base of healthy control plants and

healthy and affected plants in the highest treatment plot (0.6 pounds active ingredient per acre).
USDA Forest Service Proceedings RMRS-P-21. 2001 223

Impact of Tebuthiuron on Biodiversity of High Elevation Mountain Big Sagebrush Communities Wachocki, Sondossi, Sanderson, Webb, and McArthur

The low ammonium oxidizer populations detected in the

present study could be attributed to inhibition of ammonium-sensitive fractions (Phillips and others 2000; Suwa

and others 1994) in the media used to determine MPN and

the low number of ammonium oxidizers in semiarid land in

general. Hence, our data do not represent total ammonium

oxidizers, but only the populations that are not adversely

affected by the 0.5 g/l ammonium used in the medium

(Schmidt and Belser 1982). The apparent absence of ammonium oxidizers in some samples determined by MPN in

ammonium medium could be misleading. It is likely that the

removal of nitrate, as it is produced from further oxidation

of nitrite, is responsible for these results. The consistency

of data obtained from control and the highest treated

plots indicate that tebuthiuron does not affect ammonium

oxidizers.

Although the present study did not determine microbial

composition of samples or a profile of microbial diversity, the

results of the comparison of total heterotrophic counts and

nitrifying activity contribute to the available data on the

possible ecological impacts of tebuthiuron.

Due to the fact that tebuthiuron is an herbicide, there is

reason to suspect that it may have possible adverse effects on

photosynthetic microbial populations in treated soil. The

role of cyanobacteria and algae in nitrogen fixation and the

cryptogamic crust structure is well known. However, there

is limited information regarding the impact of tebuthiuron

on green algae. Price and others (1989) studied its effects on

green algae found in playa lakes. This study indicated that

runoff from agricultural fields treated with tebuthiuron

concentrations greater than 2.24 kg AI per ha may adversely

affect the green algae communities of playa lakes. To our

knowledge, there are no studies addressing the effect of

tebuthiuron on photosynthetic microorganisms in the soil.

There were no significant differences between photosynthetic microbial population sizes at each site when the MPN

of the highest treated and control plots were compared. The

results may even suggest a slight increase in treated sites by

the end of the third year. Therefore, in the absence of data to

assess photosynthetic microbial populations in all 3 years,

we could only conclude that tebuthiuron does not have a

lasting effect at concentrations used in this study.

The results indicate that understory vegetation is not

affected after 3 years and that all plant species sampled

show mycorrihzal associations. Therefore, one could conclude that mycorrhizal fungi in the soil and their associations are not affected by tebuthiuron application.

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224 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Susan E. Meyer is a Research Ecologist and Susan C. Garvin is a

Biological Technician, USDA Forest Service, Rocky Mountain Research

Station, Shrub Sciences Laboratory, 735 North 500 East, Provo, UT 84606.

Julie Beckstead is a Postdoctoral Research Associate, Department of Ecology and Evolutionary Biology, University of California at Santa Cruz, Earth

and Marine Sciences Building, 1156 High Street, Santa Cruz, CA 95064.

Abstract—Cheatgrass (Bromus tectorum) has recently displaced

salt desert shrubland in many areas of the Great Basin. We studied

the dynamics of cheatgrass invasion into an intact shadscale-gray

molly community in Dugway Valley, Utah, by adding seeds and

manipulating disturbance regime and resource availability. Shrub

clipping or cryptobiotic crust trampling on large plots increased

cheatgrass recruitment and biomass production slightly in a favorable moisture year (1997 to 1998), whereas in a less favorable

moisture year (1998 to 1999) these disturbance treatments had a

significant negative effect. In 1998 to 1999 small plot studies,

recruitment was similar in intact shrub clumps and openings, but

biomass and, therefore, seed production was three times greater in

shrub clumps. Disturbance decreased recruitment but had no significant effect on biomass per plant. Added water had no effect in

openings, but added N increased and reduced N decreased biomass.

In shrub clumps, fertility manipulation had little effect, but added

water increased biomass. Shrub simulation (water + N + shade)

increased biomass per plant in openings, whether intact or disturbed. It had no effect in shrub clumps where shrubs were intact,

but caused a large increase in both recruitment and biomass per

plant where shrubs were removed. Shrub clumps provide foci of

invasion because of their higher resource availability, but the

shrubs have competitive as well as facilitative effects. In a dry year

(1999 to 2000), there was no survival to reproduction in any

treatment. There are no intrinsic obstacles to cheatgrass invasion at

this site, but the process will be very slow because of low site

productivity and the high probability of drought years. Disturbance

is not a necessary precondition for invasion, but may facilitate the

process in favorable years.

Introduction ____________________

Shrub steppe ecosystems of the Great Basin are in the

process of a massive type conversion to low diversity annual grasslands heavily dominated by the exotic annual

cheatgrass (Bromus tectorum). Fire frequency is a key factor

in this conversion. The importance of fire in shrub steppe

Factors Mediating Cheatgrass Invasion

of Intact Salt Desert Shrubland

Susan E. Meyer

Susan C. Garvin

Julie Beckstead

ecosystems depends on several factors. The long-term importance of infrequent but recurring fire in maintaining

mosaics of shrub and perennial grass domination has been

established for sagebrush steppe ecosystems (Peters and

Bunting 1994). But overgrazing accompanied by invasion of

exotic annual grasses that form a continuous layer of fine

fuel has drastically increased fire frequency in these ecosystems, with fire return times decreasing from 50 to 200 years

to 3 to 5 years (Whisenant 1990). This has resulted in

complete loss of the shrub overstory and establishment of an

annual grass dysclimax that perpetuates itself through

repeated burning on ever-increasing areas (Billings 1994;

D’Antonio and Vitousek 1992).

Shadscale-dominated ecosystems, which generally occur

in areas of lower precipitation than sagebrush steppe ecosystems, experienced fire very infrequently if at all prior to the

introduction of exotic annuals in the understory (West

1994). These ecosystems have been heavily impacted by a

century and a half of livestock grazing and weed invasion,

and few if any truly pristine areas exist. But the impact of

fire in salt desert shrublands has manifested itself only

recently, within the last 25 years (West 1994). The relatively

sudden appearance of fire as a factor was associated with an

increase in density and biomass production of cheatgrass

that may already have been present in the understory. No

one knows exactly what happened to open shadscale communities to massive understory dominance by cheatgrass,

but a sequence of years of exceptionally high precipitation in

the early 1980s is implicated in the effect. The result has

been a rapid and extensive type conversion to a cheatgrass

dysclimax with short fire return times, similar to the type

conversion so widespread in sagebrush steppe ecosystems.

The question addressed in the work described here is how

shadscale communities are placed at risk for understory

takeover by cheatgrass, and whether there is any way to

minimize this risk. We need to know how difficult it will be

to manage these ecosystems as shrublands in the long term,

and whether it is possible to restore shadscale ecosystems to

a state that can resist massive annual grass invasion. This

study represents a necessary step toward answering those

questions.

One problem with descriptive studies of plant community

change is difficulty in separating the effects of multiple

causal factors. For example, heavy livestock grazing in a

shadscale community can have many effects, including destruction of the cryptobiotic soil crust through trampling,

selective elimination of palatable understory perennials,

prevention of shadscale seed banking through consumption

of fruits, and introduction of weed seeds. These in turn may

have different effects on weed invasion success. In our
USDA Forest Service Proceedings RMRS-P-21. 2001 225

Factors Mediating Cheatgrass Invasion of Intact Salt Desert Shrubland Meyer, Garvin, and Beckstead

experimental study, we introduced each of several factors

independently, making it possible to examine the effect of

each factor on invasion success, both alone and in combination. The study had two principal objectives: first, to determine the effect of seed introduction and systematic disturbance of an intact shadscale community on cheatgrass

success, and second, to determine whether the effects of

disturbance on cheatgrass success are mediated through soil

nitrogen and/or water availability.

Study Site Description ___________

Shrub steppe ecosystems dominated by shadscale (Atriplex

confertifolia) occupy millions of acres in the Great Basin

(Stutz 1978; Blauer and others 1976). Although referred to

as salt desert shrublands, shadscale communities occur on

fine-textured soils that are variably saline, in the zone

between the greasewood (Sarcobatus vermiculatus) communities of the playa bottoms and the sagebrush (Artemisia

tridentata and A. nova) communities of less xeric upland

sites with coarser soils (Billings 1949).

The Camelback study site is located at an elevation of

1,310 m in Dugway Valley, on the Dugway Army Proving

Grounds, approximately 170 km west of the Wasatch Front

urban area. The army facility at Ditto is approximately 3 km

to the north, and Camelback Hill is a few kilometers to the

south. The vegetation on the site is a shrubland with shadscale

(Atriplex confertifolia) and gray molly (Kochia americana) as

the dominant species, and with a vascular plant cover value

of 22 percent (Meyer and Garvin, unpublished data). Herbaceous perennial understory is essentially lacking. All surfaces, whether under shrubs or in openings, are inhabited by

a well-developed cryptobiotic crust made up of lichens,

mosses, and cyanobacteria. Weedy annuals present on the

study site include perfoliate pepperweed (Lepidium

perfoliatum) and bur buttercup (Ranunculus testiculatus),

principally in the openings. In summer 1997, the only

evident cheatgrass was along gravelly road shoulders, though

there was a large population in a flooding area next to a

gravel road a few hundred meters away.

The average annual precipitation at the study site, based

on a station at nearby Ditto, is 208 mm (8.19 inches; table 1).

The site has a history of sheep grazing but has been protected from grazing by livestock for over 50 years. Feral

horses and pronghorn have access to the area but rarely

visit. There is minimal vehicular disturbance.

Soils at the site are generally calcareous clay loams of

moderately alkaline pH and moderate salinity and sodicity.

In samples collected in November 1997, salinity, clay content, and carbonate content increased significantly with

depth, while pH and sodicity (as measured by sodium adsorption ratio) did not (table 2). None of these parameters

Table 1—Monthly long-term precipitation totals and 1998, 1999, and

2000 water year (October 1 to September 30) monthly totals

in millimeters at the Ditto Weather Station.

Month WY1998 WY1999 WY2000 Longterm

October 15 45 0 20

November 26 8 1 15

December 10 6 1 15

January 14 25 19 12

February 41 5 29 14

March 44 5 4 21

April 21 52 8 21

May 16 28 20 26

Season totala 187 174 82 144

June 60 27 — 15

July 25 3 — 14

August 13 8 — 15

September 18 12 — 20

Grand total 303 224 — 208

a

Total for 8-month season of growth for cheatgrass, a winter annual that

emerges in autumn, winter, or early spring and matures by early summer.

Table 2—Mean values and significance tests for 10 soil parameters measured at 0 to 15 cm and 15 to 30 cm depths under shrub canopies and in

openings at the Camelback study site. N = 4 per treatment combination.

Under shrubs In openings Probability of significance from ANOVA

Surface Sub-surface Surface Sub-surface Shrub versus Surface versus Shrub/opening x

Parameter (0 to 15 cm) (15 to 30 cm) (0 to 15 cm) (15 to 30 cm) opening subsurface surface/subsurface

Nitrate-N (ppm)a 12.2 7.6 6.9 6.8 <0.02 <0.06 <0.07

P (ppm)b 14.3 14.0 16.4 9.8 ns ns ns

K (ppm)a 704 818 809 867 <0.05 <0.06 ns

Org. Matter

 (percent) c 1.17 1.38 0.99 1.30 <0.06 <0.01 ns

Elec.Cond.

 (mmhos/cm)a 5.4 8.9 5.1 10.3 ns <0.001 ns

pHa 7.9 7.9 7.8 8.0 ns ns ns

Sodium ARa 27.1 34.2 28.8 37.0 ns ns ns

Carbonate

 (percent)d 35.0 41.3 33.2 41.4 ns <0.0001 ns

Sand (percent) 36.2 24.9 38.4 21.8 ns <0.0001 ns

Clay (percent) 44.4 62.1 41.6 63.3 ns <0.0001 ns

a

In saturation extract.

b

Bicarbonate-extractable.

c

Walkley-Black method.

d

Calcium carbonate equivalent.
226 USDA Forest Service Proceedings RMRS-P-21. 2001

Meyer, Garvin, and Beckstead Factors Mediating Cheatgrass Invasion of Intact Salt Desert Shrubland

differed significantly between shrub clumps and openings.

Organic matter was generally low but was higher in shrub

clumps and increased with depth, probably because of the

high root:shoot ratios of the dominant shrub species

(Holmgren and Brewster 1972). Phosphorus and potassium

were present in nonlimiting amounts. Phosphorus concentration was not related to position or depth, while potassium

was significantly higher in the subsoil and in openings.

Nitrate-N was present at low levels, as would be expected

with the low organic matter content. It was higher in shrub

clumps than in openings and higher in the surface soil than

in the subsoil. Nitrate-N was 50 percent higher in the

surface soil under shrubs than in the open or in the subsoil.

Surface soils under shrub clumps were also less compacted

than soils in openings, with more surface roughness and

lower bulk density.

Materials and Methods ___________

Field experiments were initiated in September of each

year. Disturbance studies utilizing large plots were carried

out in 1997 to 1998, 1998 to 1999, and 1999 to 2000, while

small plot resource manipulation studies were performed

for 2 years starting in September 1998. Cheatgrass seeds

were collected on the Whiterocks Road in former shadscale

vegetation, ca. 28 km northeast of the study site, in June of

each year, cleaned to >95 percent purity, tested for viability,

and allowed to after-ripen under laboratory conditions until

the broadcast planting without any covering treatment in

September.

The large plot study initiated in 1997 consisted of four

disturbance treatments, two seeding treatments, and 10

blocks for a total of eighty 1 x 3 m plots. The disturbance

treatments included: intact shrubs and crust, shrubs clipped

and left in place, crust trampled in place, and shrubs clipped

in combination with crust trampled. The seeding treatments

were no additional seed and 100 viable seeds (florets) per

0.1 m2

. This design was repeated the following 2 years with

the exception that unseeded plots were not harvested, so

that the plot total was 40. The same plots were used each

year, with reclipping of any resprouted shrubs and

redisturbance of the crust.

The small plot study was also a randomized block design,

with eight replications. The treatment design was factorial

with two positions (shrub clumps and openings), two disturbance treatments (intact and removal), and six resource

manipulation treatments, for a total of 24 treatment combinations and 192 plots. The manipulations included: control,

added water, added shade, added nitrogen, reduced nitrogen

(by adding sucrose to immobilize nitrogen into microbial

biomass), and shrub simulation (added shade, nitrogen, and

water). Plot size was 0.1 m2

; the same plots were used each

year.

Living shadscale shrubs >50 cm in crown diameter were

selected for the shrub clump treatments. For the removal

treatment, shrubs were clipped at ground level. Cryptobiotic

crust was left intact in the shrub removal plots. For the open

removal treatment, the cryptobiotic crust was physically

removed to a depth of ca. 2 cm.

For the supplemental water treatment, water was added

to simulate 25 mm of extra rainfall in mid-October and

mid-March by suspending water-filled ziplock bags on hardware cloth platforms over the plots and allowing the water

to drip through holes punched in the bottoms. Application

took approximately an hour and resulted in little or no

runoff. Nitrogen was added at a rate of 5.3 g per m2 per yr in

the form of ammonium nitrate, while sucrose was added at

a rate of 50 g per m2 per yr (McLendon and Redente 1992).

Fertility treatments were applied dry at the same time as

supplemental watering in the fall and spring, and plots were

watered with a few milliliters of water to help prevent

removal by wind. Shade was continuously applied through

the course of the study by surrounding each shade plot with

a quadrangular frame covered with 2 mm fiberglass window screening to a height of 45 cm. The shade frame tops

were open.

Harvest took place in May each year after the plants had

turned red and the seeds had reached maximum dry mass,

but before any seed shatter. The first year, plants in the

large plot experiment were counted after harvest, then dried

at 40 °C for 48 hours and weighed to obtain total biomass per

plot. In following years, only total biomass per plot was

measured. For the small plot study, plants for each plot were

counted during harvest and separated into seed (floret) and

vegetative fractions. Each fraction was then dried and

weighed to obtain biomass as above. Biomass per plant was

a good predictor of seed biomass and, therefore, of seed

number (R2 = 0.965, d.f. = 190, p < 0.0001)

All count and biomass data were log-transformed prior to

analysis of variance to increase homogeneity of variance

(Zar 1984). Dependent variables for all analyses included

number of plants setting seed per 0.1 m2

, dry biomass per

0.1 m2

, and biomass per plant. For the small plot study, seed

fraction (floret mass/total mass) was also included. After

determining that the block effect was not significant for any

variable, it was pooled into the error term, and the data were

analyzed as completely randomized designs. Data for the

1998 and 1999 large plot harvests were analyzed separately

using fixed-effects two-way (1999 and 2000) or three-way

(1998) analysis of variance. Data for the 1999 small plot

study were analyzed as three-way fixed-effects models

using a general linear models procedure. Control treatments for the four shrub/open intact/removal small plot

treatment combinations were then compared with each

other and with their respective manipulation treatments

using orthogonal contrasts (Steel and Torrie 1980).

Results ________________________

Large Plot Study

The 1997 to 1998 fall-winter-spring season was favorable

for cheatgrass at the Camelback study site, with adequate

autumn, winter, and spring precipitation (table 1). Estimated seed return on the seeded plots averaged 28 percent,

with 28 plants reaching reproductive maturity and mean

biomass production of 1.2 g per 0.1 m2 on seeded plots.

Cheatgrass success in 1997 to 1998 was clearly limited by

seed supply (table 3). There were 10 times as many plants on

the seeded plots, and they produced five times as much

biomass as the plants on the unseeded plots (fig. 1). The

plants on the unseeded plots averaged twice the size of

those on the seeded plots, however.
USDA Forest Service Proceedings RMRS-P-21. 2001 227

Factors Mediating Cheatgrass Invasion of Intact Salt Desert Shrubland Meyer, Garvin, and Beckstead

Disturbance treatments had a slight but significant

effect on cheatgrass success on the large plots in 1997 to

1998, and the effects were similar in seeded and unseeded

plots (table 3). Plants were 30 percent larger overall where

shrubs were left intact (table 3, nearly significant), but mild

disturbance (either clipping or trampling but not both)

resulted in a ca. 30 percent increase in recruitment and a

ca. 20 percent increase in biomass per 0.1 m2 (table 3,

significant shrub treatment by crust treatment interactions;

fig. 1). The severe disturbance treatment (shrubs clipped

and crust trampled) did not show this beneficial effect, with

numbers similar to those on intact plots and total biomass

lower than any other treatment (fig. 1).

The 1998 to 1999 season was less favorable for cheatgrass

at Camelback, with little late winter moisture (table 1).

Biomass per 0.1 m2 in the large plot study averaged only

0.262 g overall, little more than one-fifth of the value on

seeded plots the previous year. In intact plots, biomass

production was three times greater in 1998 than in 1999.

Under this weather scenario, disturbance had a clear negative effect on biomass production, with the effects of both

shrub clipping and crust trampling significant (table 2;

fig. 2). Biomass production in the severe disturbance treatment was decreased by a factor of three relative to the intact

plots.

The 1999 to 2000 season was categorically unfavorable for

cheatgrass at Camelback, due to unusually dry conditions

(table 1). Recruitment was minimal and no plants survived

to reproduction, regardless of treatment, in either the large

plot study or the small plot study described below.

Small Plot Study

Analysis of the 1999 harvest data for the small plot study

showed that the shrub versus open treatment, the intact

versus disturbed treatment, and the manipulation treatment main effects were all significant for plant number and

total biomass per plot, but the intact versus removal treatment had no significant effect on plant size (table 4).

Table 3—Analysis of variance for the 1998 and 1999 harvests of the large plot experiment. Data were log

transformed to increase homogeneity of variance prior to analysis. The block effect was not

significant for any dependent variable: therefore, block and block interactions were pooled as the

error term. Error degrees of freedom: 1998 = 62, 1999 = 36.

Plant number Plant biomass Total plot biomass

d.f. F P FP FP

1998 experiment

Seeded/unseeded 1 197.8 0.0001 58.3 0.0001 121.0 0.0001

Shrubs intact/clipped 1 0.1 ns 3.71 0.06 1.06 ns

Crust intact/trampled 1 0.57 ns 0 ns 0.57 ns

Seeding x clipping 1 0.10 ns 1.44 ns 0.88 ns

Seeding x trampling 1 0.31 ns 0.85 ns 1.05 ns

Clipping x trampling 1 4.35 0.05 0.02 ns 4.30 0.05

Seed x clip x tramp 1 0.42 ns 0.48 ns 1.05 ns

1999 experiment

Shrubs intact/clipped 1 — — — — 17.84 0.0002

Crust intact/trampled 1 — — — — 8.11 0.0072

Interaction 1 — — — — 1.00 ns

Figure 1—Plant number per 0.1 m2 area,

dry biomass per plant, and total dry biomass per 0.1 m2 area for the large plot 1998

harvest. Disturbance treatments: intact (no

disturbance), clipped (shrubs clipped at

ground level), trampled (cryptobiotic crust

trampled) and clp + trm (shrubs clipped in

combination with crust trampled). Seeding

treatments: seeds broadcast sown at 100

per 0.1 m2 and no added seeds. See table

3 for significance tests.
228 USDA Forest Service Proceedings RMRS-P-21. 2001

Meyer, Garvin, and Beckstead Factors Mediating Cheatgrass Invasion of Intact Salt Desert Shrubland

Patterns for control plots were generally similar to patterns from the overall analysis, although sometimes not

significant.

For plant number per plot, control and overall values were

similar in shrub clumps and openings (fig. 3). Plant number

was generally negatively impacted by disturbance, a result

similar to the large plot study result from the same harvest

year. This negative impact was greater in openings, resulting in a significant shrub clump versus opening intact

versus removal interaction (table 4; fig. 3).

Biomass per plant was more than twice as high overall in

shrub clumps as in openings, and this difference was even

greater when intact control treatments were compared

(table 4; fig. 4). The removal treatment had no significant

effect on plant biomass overall in either shrub clumps or

openings.

As a result of the interplay of the above two variables,

biomass per 0.1 m2 plot was significantly higher in shrub

clumps than openings and significantly higher in intact

plots than in removal plots overall (table 4; fig. 5). Total

biomass was less impacted by disturbance in shrub clumps

than in openings, resulting in a significant interaction for

this variable. Control plots followed the same trends.

Table 4—Analysis of variance for the 1999 harvest of the small plot factorial experiment. Data (except for seed fraction) were log transformed to

increase homogeneity of variance prior to analysis. The block effect was not significant for any dependent variable; therefore, block and

block interactions were pooled as the error term. Error degrees of freedom = 165.

Number of plants Plant biomass biomass Total plot biomass Seed fraction

d.f. F P F P F P FP

Shrub versus open 1 20.01 0.0001 237.2 0.0001 97.96 0.0001 4.77 0.0307

Intact versus removal 1 20.63 0.0001 0.67 ns 11.28 0.0010 4.41 0.0373

Manipulation 5 2.82 0.0178 18.88 0.0001 8.77 0.0001 9.03 0.0001

Shrub/open x intact/rem 1 19.07 0.0001 0.52 ns 10.61 0.0014 3.02 ns

Shrub/open x manip. 5 1.22 ns 8.09 0.0001 1.14 ns 7.70 0.0001

Intact/remove x manip. 5 2.09 ns 0.81 ns 1.93 ns 0.64 ns

Sh/op x int/rmv x manip. 5 0.66 ns 1.62 ns 1.22 ns 2.66 0.0427

Figure 2—Total dry biomass per 0.1 m2 area for the

large plot 1998 and 1999 harvests. Disturbance treatments: intact (no disturbance), clipped (shrubs clipped

at ground level), trampled (cryptobiotic crust trampled),

and clp + trm (shrubs clipped in combination with crust

trampled). See table 3 for significance tests.

Only two manipulations significantly impacted plant

number per plot, and these impacts were only sometimes

evident. Shrub simulation had no effect on recruitment in

intact shrub clumps, but had a large positive effect when

shrubs were removed (fig. 3). Shrub simulation had no effect

on recruitment in openings. Shade negatively impacted

recruitment in openings but not in shrub clumps.

Biomass per plant was positively affected by supplemental water in shrub clumps, whether shrubs were intact or

removed (fig. 4). Supplemental water had no effect on biomass per plant in openings. Conversely, added nitrogen

increased and sucrose decreased biomass per plant in openings, but had no effect in shrub clumps. Shrub simulation

(water + nitrogen + shade) had no effect in intact shrub

clumps but a large positive effect when shrubs were removed. It had a significant positive effect on biomass per

plant in openings whether or not crust was removed.

No manipulation treatment resulted in significantly increased biomass per plot relative to the control when

shrubs were intact. With shrubs removed, shrub simulation had a large positive effect, while the positive effect of

supplemental water alone was nearly significant (fig. 4). In

openings, shrub simulation increased total biomass significantly over the control only when the crust was intact,

although a similar but nonsignificant trend was evident in

the removal treatment.

Seeds (florets) made up 29 to 48 percent of total dry

mass, with a mean of 43 percent. Seed investment was

significantly higher in shrub clumps than in openings and

in intact versus removal treatments, although the differences in investment were not large (table 4; fig. 5). In

control treatments, seed investment was higher in intact

shrub clumps than in the other three treatments, and there

was no significant manipulation effect with shrubs intact,

although sucrose addition tended to reduce reproductive

investment. With shrubs removed, added nitrogen decreased reproductive investment. In openings, which showed

nitrogen limitation on plant biomass, added nitrogen had a

null or positive effect on reproductive investment, while

nitrogen depletion through sucrose addition resulted in a

sharp decrease.

As mentioned above, the harvest for the 1999 to 2000 year

in the small plot study was zero, regardless of position,

disturbance treatment, or manipulation. There were, therefore, no significant treatment effects or interactions for any

dependent variable.
USDA Forest Service Proceedings RMRS-P-21. 2001 229

Factors Mediating Cheatgrass Invasion of Intact Salt Desert Shrubland Meyer, Garvin, and Beckstead

Figure 3—Plant number per 0.1 m2 plot for

each treatment combination in the small

plot 1999 harvest. Control treatments with

means not significantly different at the p <

0.05 level have columns headed by the

same letter. Manipulation treatments that

are significantly different from the control

manipulation treatment within a shrub/open

intact/removal treatment combination have

columns headed by asterisks (*, p < 0.05;

**, p < 0.01, ***, p < 0.001; o, p < 0.10,

marginally significant; CTR, control; S SIM,

shrub simulation; H20, supplemental water; N, supplemental nitrogen; SUG, sucrose addition to reduce available nitrogen;

SHADE, plots shaded).

Figure 4—Dry biomass per plant for each

treatment combination in the small plot

1999 harvest. Control treatments with means

not significantly different at the p < 0.05 level

have columns headed by the same letter.

Manipulation treatments that are significantly different from the control manipulation treatment within a shrub/open intact/

removal treatment combination have

columns headed by asterisks (*, p < 0.05;

**, p < 0.01, ***, p < 0.001; o, p < 0.10,

marginally significant; CTR, control; S SIM,

shrub simulation; H20, supplemental water; N, supplemental nitrogen; SUG, sucrose addition to reduce available nitrogen;

SHADE, plots shaded).
230 USDA Forest Service Proceedings RMRS-P-21. 2001

Meyer, Garvin, and Beckstead Factors Mediating Cheatgrass Invasion of Intact Salt Desert Shrubland

Figure 5—Total dry biomass per 0.1 m2

plot for each treatment combination in the

small plot 1999 harvest. Control treatments

with means not significantly different at the

p < 0.05 level have columns headed by the

same letter. Manipulation treatments that

are significantly different from the control

manipulation treatment within a shrub/open

intact/removal treatment combination have

columns headed by asterisks (*, p < 0.05;

**, p < 0.01, ***, p < 0.001; o, p < 0.10,

marginally significant; CTR, control; S SIM,

shrub simulation; H20, supplemental water; N, supplemental nitrogen; SUG, sucrose addition to reduce available nitrogen;

SHADE, plots shaded).

Figure 6—Fraction of dry mass invested

in seeds (florets) for each of 24 treatment

combinations in the small plot 1999 harvest. Control treatments with means not

significantly different at the p < 0.05 level

have columns headed by the same letter.

Manipulation treatments that are significantly different from the control manipulation treatment within a shrub/open intact/

removal treatment combination have columns headed by asterisks (*, p < 0.05; **,

p < 0.01, ***, p < 0.001; o, p < 0.10,

marginally significant; CTR, control; S SIM,

shrub simulation; H20, supplemental water; N, supplemental nitrogen; SUG, sucrose addition to reduce available nitrogen;

SHADE, plots shaded).
USDA Forest Service Proceedings RMRS-P-21. 2001 231

Factors Mediating Cheatgrass Invasion of Intact Salt Desert Shrubland Meyer, Garvin, and Beckstead

Discussion _____________________

There appears to be little intrinsic resistance to cheatgrass

invasion at the Camelback study site, in spite of its aridity,

heavy soils, and high salinity. Seed supply or propagule

pressure is the principal extrinsic factor mediating invasion rate. Resource availability determines the rate of

recruitment from arriving propagules, and also regulates

plant size and, therefore, seed production per plant. The

degree of availability of “excess” resources to support

cheatgrass recruitment and growth is related to effective

precipitation and fluctuates from year to year (Davis and

others 2000). The probable reasons that cheatgrass has not

yet extensively invaded this plant community in Dugway

Valley are at least twofold. First, dispersal into the area is

minimized because human traffic is generally excluded or

at least closely regulated, and herbivores that could transport seeds rarely enter this community type. Second,

invasibility is greatly reduced in perhaps a majority of

years by resource limitation related to the low and sporadic

precipitation.

Recruitment from arriving propagules varied from 0 to

28 percent in our study. If we use 0.003 g as the average

mass of a single cheatgrass propagule (Meyer, unpublished

data), we can estimate seed production per plant from total

biomass and seed investment values. In the 1997 to 1998

large plot study, plants in seeded plots averaged 0.050 g and

produced an estimated seven seeds. At a return on seed for

the following year of 24 percent (from 1998 to 1999 small

plot study), those seven seeds would produce 1.7 plants, less

than a doubling of the population. If we assume that in 1998

to 1999 recruitment was similar on intact large and small

plots, namely 24 percent, then an individual plant on intact

large plots would have averaged 0.016 g and would have

produced 2.3 seeds. Given an optimistic return on seed for

the following year of 25 percent, those seeds would produce

on average 0.6 plants. Under this scenario, the population

would experience no net growth across these three relatively

favorable years.

In fact, the return on seed for 1999 to 2000 was much less

than 25 percent; it was effectively zero. If all the seeds in the

seed bank germinated but failed to survive, that would put

the cheatgrass population at zero until the immigration of

more seeds. An unknown fraction of the seeds produced in

1999 may have survived in the seed bank, although seed

bank carryover is positively related to cheatgrass litter cover

and, therefore, probably minimal at this site (Beckstead

2001). But even if, say, half of the seeds survived, the

population would still be declining sharply, because recruitment from remaining seeds is not likely to exceed 25 to 30

percent, even in the most favorable year. This means that it

would take a very unusual series of favorable water years to

cause an exponential increase in cheatgrass biomass at

this site.

Cheatgrass plants that occurred in intact shrub clumps

in the 1999 small plot study were three times the size of

those in openings and produced even more than three times

as many seeds because of their higher reproductive investment. Even with an artificially equal initial distribution of

propagules in the large plots and a shrub cover of 22

percent, almost as many seeds were produced in shrub

clumps as in openings. Supplemental water increased this

size advantage in shrub clumps. These facts may explain

why plants in the unseeded plots in 1998 were twice as big

as those in the seeded plots. Though we have no quantitative data to support this observation, it was clear that most

of the plants in the unseeded plots were in shrub clumps.

This would represent the natural invasion pattern. Shrub

clumps are the foci of invasion because of their greater

resource availability and the resulting increase in seed

production per plant. Because 1998 was a more favorable

water year than 1999 and because cheatgrass plants in

shrub clumps respond more to additional water, the differential size advantage in shrub clumps would have been

even greater in 1998. The shrubs apparently act as nurse

plants for cheatgrass, ameliorating growing conditions for

this understory species in an otherwise harsh environment, an effect commonly observed in warm desert ecosystems (Franco and Nobel 1989). The shrub clumps act as

“fertile islands” surrounded by less productive openings

(Garner and Steinberger 1989).

The impact of disturbance in opening the Camelback site

to cheatgrass invasion was disappointingly small. In the

most favorable water year, moderate disturbance (either

trampling or clipping but not both) increased recruitment by

30 percent, and it increased biomass production and, therefore, seed production by 20 percent, but more severe disturbance (both trampling and clipping) had a null or negative

effect. In a less favorable year, disturbance of any kind had

a negative effect on cheatgrass biomass production. Disturbance is, therefore, not necessary for cheatgrass invasion at

the Camelback site, but may speed the invasion process in

favorable water years. This could have impact, because

favorable water years are the only years when there can be

net cheatgrass population growth at this site.

Because of low cheatgrass biomass and seed production

even in favorable years, it may be hard to see how openings

at Camelback could ever support closed stands of cheatgrass

(Beckstead 2000). This would limit disturbance from fire,

because the fuel would remain discontinuous even in high

water years. But cheatgrass dominance results in a redistribution of organic matter and fertility from the subsurface to

the surface (Meyer and Garvin, unpublished data). Heavy

cheatgrass production in shrub clumps over a period of

unusually wet years could result in a gradual encroachment

and eventual coalescing of litter across the openings, resulting in less N limitation and more favorable soil physical

characteristics for cheatgrass production. We have seen this

process occurring in heavily invaded shadscale communities

in adjacent, less xeric, Skull Valley. Once this happens,

cheatgrass can thrive in the openings, the fuel can become

continuous, and the vegetation can carry fire.

The shrub simulation treatment with shrubs removed

dramatically increased cheatgrass recruitment and biomass

production. This treatment may mimic what happens after

a shadscale plant dies. The soil and microsite characteristics

that make shrub clumps more favorable persist and, in the

case of fertility, may even be enhanced in the years after

shrub death, making dead shrub clumps highly favorable

microsites for cheatgrass. This effect became important on a

landscape scale in the early 1980s, when the same series of

high water years that speeded cheatgrass invasion also

resulted in widespread shadscale stand loss (Nelson and

others 1990). Stand loss itself does not result in local
232 USDA Forest Service Proceedings RMRS-P-21. 2001

Meyer, Garvin, and Beckstead Factors Mediating Cheatgrass Invasion of Intact Salt Desert Shrubland

extinction, because shadscale is able to recruit from a persistent seed bank (Meyer and others 1998). But the concomitant increase in cheatgrass biomass production within these

communities greatly increases the probability of recurring

fire and rapid conversion to cheatgrass domination.

This scenario was not played out in Dugway Valley as it

was in many other eastern Great Basin desert valleys,

principally because of its greater aridity and seed limitation.

The probability that cheatgrass will eventually take over

and displace shadscale communities in Dugway Valley depends on weather patterns as well as on seed availability.

The best hope for protecting the salt desert shrub communities in Dugway Valley, therefore, lies in reducing the probability of propagule arrival by restricting entry and by

eradicating adjacent populations, as well as limiting levels

of anthropogenic disturbance.

Acknowledgments ______________

This research was supported by Rangelands Special Grant

CSREES 97-38300-4576. The study site was made available

through a Memorandum of Understanding between the

Shrub Sciences Laboratory and the U.S. Army Dugway

Proving Grounds. Soils analyses were provided by Bruce

Webb, Brigham Young University, Department of Agronomy

and Horticulture. Thanks to the following for field assistance: Stephanie Carlson, Suzette Clement, Ajmal Khan,

Kerry Mitchell, Alisa Ramakrishnan, and Bitsy Schultz.

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Lance T. Vermeire is a Research Assistant and Robert B. Mitchell is an

Assistant Professor of Range Management, Department of Range, Wildlife,

and Fisheries Management, Texas Tech University, Lubbock, TX 79409.

Samuel D. Fuhlendorf is an Assistant Professor of Rangeland Ecology, Plant

and Soil Sciences Department, Oklahoma State University, Stillwater, OK

74078.

Sand Sagebrush Response to Fall

and Spring Prescribed Burns

Lance T. Vermeire

Robert B. Mitchell

Samuel D. Fuhlendorf

Abstract—Sand sagebrush (Artemisia filifolia) is a dominant shrub

on sandy soils throughout the Great Plains and Southwest. Sand

sagebrush is reported to reduce wind erosion and provides valuable

forage and cover to numerous wildlife species. However, the fire

ecology of sand sagebrush is not well understood. Our objectives

were to evaluate fire-induced mortality, occurrence of resprouting,

and changes in sand sagebrush canopy structure and total nonstructural carbohydrates (TNC) following fall and spring prescribed

burns. We selected twelve 4-ha plots on sand sagebrush-dominated

sites in high-seral sand sagebrush-mixed prairie near Woodward,

OK. Four plots were burned during fall, four were burned during

spring, and four served as controls. Soil temperature and soil water

content were monitored. About 93 percent of burned shrubs

resprouted and TNC was similar across burning treatments. Canopy

volume in May was reduced 87 and 99 percent by fall and spring

burns, respectively. Fall burning had no effect on soil water content

and elevated soil temperature only during April and May. Springburned plots had greater soil water content and higher soil temperatures than control plots in May.

Introduction ____________________

Sand sagebrush (Artemisia filifolia) is a dominant climax

shrub on sandy soils from South Dakota through northern

Mexico and eastern Nevada through western Oklahoma.

Sand sagebrush has high potential for reducing wind erosion

(Hagen and Lyles 1988) and provides valuable forage for

numerous wildlife species and occasionally livestock. The

shrubs also provide important nesting and protective cover

for lesser prairie chickens (Tympanuchus pallidicinctus)

and other upland game birds (Cannon and Knopf 1981).

However, the ecological impact of burning sand sagebrush is

not well documented. Sand sagebrush has been classified as

both a sprouter (Wright and Bailey 1982) and a non-sprouter

capable of recolonizing disturbed sites with abundant seedlings (Sosebee 1983; Wright 1972; Wright and Bailey 1980).

Numerical data are lacking to support either hypothesis.

Our objectives were to evaluate the effects of fall and spring

prescribed burns on (1) fire-induced mortality and occurrence of resprouting in sand sagebrush, (2) canopy structure,

(3) total non-structural carbohydrate (TNC) trends, (4) soil

water content, and (5) soil temperature.

Methods and Materials ___________

Study Area

The study was located on the Hal and Fern Cooper Wildlife

Management Area, 15 km northwest of Woodward, OK

(36° 34’ N, 99° 32’ W, elevation 640 m). The area consists of

sandhills in a high seral stage of the sand sagebrush-mixed

prairie vegetation type. The climate is continental with

602 mm average annual precipitation, 70 percent of which

occurs during the April to September growing season. The

study was conducted on deep sand ecological sites. Soils

were Pratt loamy fine sands (mixed, mesic, Psammentic

Haplustalfs) with no limiting layers of clay in the top 150 cm.

The woody plant community is strongly dominated by sand

sagebrush, with lesser amounts of Chickasaw plum (Prunus

angustifolia). Dominant grasses include little bluestem

(Schizachyrium scoparium), sideoats grama (Bouteloua

curtipendula), sand bluestem (Andropogon hallii), and sand

lovegrass (Eragrostis trichodes). Western ragweed (Ambrosia psilostachya), sand lily (Mentzelia nuda), and annual

buckwheat (Eriogonum annuum) were prominent forbs at

the time of the study.

Methods

We selected twelve 4-ha plots on sand sagebrushdominated sites. Twenty shrubs in each plot were marked

with rebar stakes, and canopy height, area, and volume were

measured in November. Four plots were burned during fall

(16 November 1999), four were burned during spring

(17 April 2000), and four served as controls. Resprouting and

canopy structure of marked plants were reevaluated in May

2000. Roots located below the bud zone were collected from

five shrubs per burn treatment each month. Total

nonstructural carbohydrates were measured colorimetrically (absorbance at 612 nm) with an anthrone reagent

(Murphy 1958) and glucose as a standard. Soil water was

determined gravimetrically from five soil cores taken monthly

to 15- and 30-cm depths at each plot. Five mid-day soil

temperature readings were recorded monthly from each plot

at 7.5 and 22.5 cm below the soil surface.
234 USDA Forest Service Proceedings RMRS-P-21. 2001

Vermeire, Mitchell, and Fuhlendorf Sand Sagebrush Response to Fall and Spring Prescribed Burns

Differences in TNC, resprouting, and canopy structure

among burn treatments were determined with t-tests. Soil

water content and soil temperature were analyzed with

analysis of variance. The model contained terms for burn

treatment, sampling depth, month (as a repeated measures

effect), and their interactions. Where differences occurred,

means were separated by the least significant difference.

Unless otherwise noted, an alpha level of 0.05 was used for

all hypothesis testing.

Results ________________________

Fire-induced mortality was less than 10 percent for fall

and spring burns (table 1). Sand sagebrush on fall-burned

plots began resprouting in March, a full month after bud

break on non-burned shrubs. Shrubs in spring-burned plots

initiated resprouting in May. However, TNC concentration

was similar among burn treatments except during January

(fig. 1). The primary effect of fire on sand sagebrush was the

alteration of canopy structure (table 1). Fall burns reduced

shrub height by nearly 50 percent, and canopy area and

volume by more than 75 percent. The same shrub canopy

measures were reduced more than 90 percent by spring

burns.

Soil water content and soil temperature were similar

among burn treatments from December through March. Soil

water was unaffected by sampling depth, but soil temperature was 2.3 °C warmer at 7.5 cm than at 22.5 cm. Springburned plots had greater soil water content across sampling

depths than fall-burned or control plots in May (table 2). Fall

burning increased soil temperature by about 17 percent in

April and May. Spring burns increased soil temperature by

16 percent in May.

Discussion _____________________

Sand sagebrush resprouts profusely following fall and

spring burns, seemingly without any negative effects on

carbohydrate reserves. Applying prescribed fire to sand

sagebrush communities does not appear to be a viable option

for reducing shrub density, unless delayed mortality occurs

due to additional stresses, such as infestation by insects.

Prescribed fire may be a useful tool for reducing sand

sagebrush canopy height and volume and potentially making resources, such as light and water, available to more

desirable grasses and forbs. Higher spring soil temperature

can be expected on burned sites if non-burned sites are

shaded by the plant canopy or sufficiently covered with

mulch. We believe soil temperatures were likely similar over

the winter because the lack of insulating plant material on

burned sites allowed solar heat captured during the day to

escape more readily at night. Similarly, increased evaporation rates on unprotected soils of burned sites may negate

gains in soil water content from reduced canopy interception. Differences in soil water content occurred when the

Figure 1—Monthly percent total nonstructural carbohydrates of sand sagebrush roots from non-burned,

fall-burned, and spring-burned shrubs.

Table 1—Percentage of sand sagebrush plants resprouting in May after fall and spring burns and percent

reduction in canopy structure.

Burn season Resprouting Canopy height Canopy area Canopy volume

Percent - - - - - - - - - - - Percent reduction - - - - - - - - -

Fall 94 a1 49 a 76 a 87 a

Spring 92 a 90 b 95 b 99 b

1

Means followed by different letters within columns are different at alpha = 0.05.

Table 2—May soil water and soil temperature in non-burned, fall-burned, and spring-burned

plots.

Soil temperature (°C)

Burn treatment Soil water (percent) 7.5 cm depth 22.5 cm depth

Control 2.2 a 1 22.6 a 16.4 a

Fall 2.0 a 27.2 b 18.5 b

Spring 3.1 b 25.9 b 19.3 b

1

Means followed by different letters within columns are different at alpha = 0.05.
USDA Forest Service Proceedings RMRS-P-21. 2001 235

Sand Sagebrush Response to Fall and Spring Prescribed Burns Vermeire, Mitchell, and Fuhlendorf

dominant plants began active seasonal growth. We suggest

the reduced soil water content on fall-burned and nonburned sites was a reflection of their higher live plant cover.

References _____________________

Cannon, R. W.; Knopf, F. L. 1981. Lesser prairie chicken densities

on shinnery oak and sand sagebrush rangelands in Oklahoma.

Journal of Wildlife Management. 45: 521–524.

Hagen, L. J.; Lyles, L. 1988. Estimating small grain equivalents of

shrub-dominated rangelands for wind erosion control. Transactions of the American Society of Agricultural Engineers. 31:

769–775.

Murphy, R. P. 1958. Extraction of plant samples and the determination of total soluble carbohydrates. Journal of the Science of Food

and Agriculture. 9: 714–717.

Sosebee, R. E. 1983. Physiological, phenological, and environmental

considerations in brush and weed control. In: McDaniel, K. C., ed.

Brush management symposium: proceedings; 1983 February 16;

Albuquerque, NM. Denver, CO: Society for Range Management:

27–43.

Wright, H. A. 1972. Shrub response to fire. In: McKell, C. M.;

Blaisdell, J. P.; Goodin, J. R., eds. Wildland shrubs symposium—

their biology and utilization: proceedings; 1971 July; Logan, UT.

Gen. Tech. Rep. INT-1. Ogden, UT: U.S. Department of Agriculture, Forest Service, Intermountain Forest and Range Experiment Station: 204–217.

Wright, H. A.; Bailey, A. W. 1980. Fire ecology and prescribed

burning in the Great Plains—a research review. Gen. Tech. Rep.

INT-77. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Forest and Range Experiment Station.

60 p.

Wright, H. A.; Bailey, A. W. 1982. Fire ecology. New York, NY:

Wiley-Interscience. 501 p.
236 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Russell Fox is Graduate Assistant and Rob Mitchell is Fire Ecologist,

Range, Wildlife, and Fisheries Management, Texas Tech University, Lubbock, TX 79409. Mike Davin is Resource Specialist, National Park Service,

Lake Meredith National Recreation Area, Fritch, TX 79036.

Managing Saltcedar After a Summer

Wildfire in the Texas Rolling Plains

Russell Fox

Rob Mitchell

Mike Davin

Abstract—Saltcedar (Tamarix spp) has invaded nearly one million

acres of riparian ecosystems in the southwestern U.S., displacing

many native species. The objectives of this study were to estimate

saltcedar mortality to summer wildfire, summer wildfire followed

by rollerchopping, and dormant season treatment with 25 percent

triclopyr to regrowth following a summer wildfire at Lake Meredith

National Recreation Area. In July 1998, more than 100 acres of

saltcedar-infested riparian area were burned. In February and

March of 1999, regrowth of 200 dormant saltcedar trees were

treated with 25 percent triclopyr in JLB oil using the basal bark

treatment method. Rollerchopping was conducted in June 1999.

Trees that were sprayed had multiple stems and were an average of

4 feet tall. Saltcedar mortality following the summer wildfire was

60.6 percent. Rollerchopping burned areas resulted in 85.1 percent

mortality. Saltcedar mortality was 89.9 percent following the February herbicide treatment and 94.5 percent following treatment in

March. Preliminary results indicate that dormant season individual plant treatment with 25 percent triclopyr following burning

is an effective method for managing saltcedar infestations. However, rollerchopping burned areas may be the most economical in

large, alluvial flood plains.

Introduction ____________________

In Texas, six species of Tamarix are found: (1) T. africana;

(2) T. aphylla; (3)T. chinensis; (4) T. gallica; (5) T. parviflora;

and (6) T. ramosissima(Correll and Johnston 1970). Saltcedar

was introduced into the eastern U.S. in the early 1800s,

escaped cultivation by late that century, and became established throughout the U.S. (Duncan 1997). Escapes from

cultivation were first reported in the 1870s and were rapidly

spreading from one watershed to another (Brotherson and

Field 1987). During these early years of introduction, saltcedar was planted to create windbreaks, provide shade,

stabilize eroding stream banks, and grown as ornamentals

(Neill 1985). Estimates in 1961 indicated that saltcedar

infestations occupied more than 900,000 acres in the U.S.

(Robinson 1965). Deloach (1991) estimated one million acres

of prime bottomland have been infested with saltcedar and

that very little understory vegetation is present. Consequently, restoring native vegetation in saltcedar-dominated

riparian areas is an important concern in the southwestern

U.S. Our objectives were to estimate saltcedar mortality to

summer wildfire, summer wildfire followed by rollerchopping,

and dormant season treatment with 25 percent triclopyr to

regrowth following a summer wildfire at Lake Meredith

National Recreation Area (LMNRA).

Methods _______________________

This study was conducted in 1999 in a saltcedar-dominated riparian area at LMNRA near Fritch, Texas. The site

was burned by a wildfire in July 1998. Daily maximum

temperatures exceeded 100 °F during the wildfire. Many

saltcedar were completely consumed by the wildfire. Regrowth of surviving plants exceeded 6 ft at the conclusion of

the 1998 growing season. Five randomly located 10 mx 10 m

plots in adjacent nonburned areas were used as estimates of

pre-fire saltcedar density. Five randomly located 10 mx 10 m

plots were used to estimate saltcedar density in burned

areas. Saltcedar mortality due to the wildfire was estimated

as the difference between saltcedar density in the nonburned

and burned areas. In June 1999, about 50 acres of burned

saltcedar was rollerchopped. Five randomly located burned

and rollerchopped 10 m x 10 m plots were used to estimate

saltcedar mortality from the combination of burning and

rollerchopping. Two dormant season applications of 25 percent triclopyr (Garlon 4) in JLB oil (vegetable oil carrier)

were applied during February and March 1999. Herbicide

treatments were applied as individual plant basal treatments to 100 fire-generated resprouts each month. Herbicide efficacy on saltcedar regrowth was evaluated 12 months

after treatment. Mortality was defined as lack of green

material or failure to produce buds 12 months after treatment.

Results ________________________

Burning resulted in 60.6 percent saltcedar mortality 12

months after the summer wildfire when comparing saltcedar

density in burned areas to adjacent nonburned areas. The

combined effect of the summer wildfire and rollerchopping

resulted in 85.1 percent saltcedar mortality as compared to

the nonburned areas. Rollerchopping fire-induced regrowth

uprooted many plants, and provided an excellent method for

increasing saltcedar mortality following the summer wildfire. The moist, sandy, alluvial soils at LMNRA provided

ideal conditions for uprooting the sprouting collar, and

exposing root material to desiccation. Additionally, rollerchopping facilitated follow-up herbicide treatments by
USDA Forest Service Proceedings RMRS-P-21. 2001 237

Managing Saltcedar After a Summer Wildfire in the Texas Rolling Plains Fox, Mitchell, and Davin

knocking down the standing dead trunks, increasing the

accessibility of remaining resprouts. An added benefit of

rollerchopping was soil disturbance, which encouraged the

establishment of early seral species in the burned and

rollerchopped areas. February and March basal stem treatments to post-fire saltcedar regrowth with 25 percent triclopyr in JLB oil resulted in 89.9 and 94.5 percent mortality,

respectively, 12 months after treatment. Preliminary results indicate that dormant season individual plant treatment with 25 percent triclopyr following burning is an

effective method for managing saltcedar infestations.

Conclusions____________________

Fire effectively reduced saltcedar density. Rollerchopping

standing dead and regrowth 11 months after burning further reduced saltcedar density, and stimulated forb growth.

The application of 25 percent triclopyr in JLB oil during the

dormant season effectively controlled saltcedar regrowth

following burning. Preliminary results indicate combining

fire, rollerchopping, and individual plant treatments with

triclopyr is an effective approach for saltcedar management.

References _____________________

Brotherson, J. D.; Field, D. 1987. Tamarix: impacts of a successful

weed. Rangelands. 9(3): 110–112.

Correll, D. S.; Johnston, M. C. 1970. Manual of the vascular plants

of Texas. Austin: University of Texas Printing.

Deloach, C. J. 1991. Saltcedar, an exotic weed of western North

American riparian areas: a review of its taxonomy, biology,

harmful, and beneficial values, and its potential for biological

control. Final Rep. USDI, Bureau of Reclamation, Lower Colorado Region, Boulder City, NV.

Duncan, K. W. 1997. A case study in Tamarix ramosissima control:

Spring Lake, New Mexico, In: Brock, J. H.; Wade, M.; Pysek, P.;

Green, D., eds. Plant invasions: studies from North America and

Europe. Leiden, Backhuys Publishers: 115–121.

Neill, W. M. 1985. Tamarisk. Fremontia.12: 22–23.

Robinson, T. W. 1965. Introduction, spread, and areal extent of

saltcedar (Tamarix) in the Western United States. U.S. Geological Survey Professional Paper 491-A.
238 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

W. K. Ostler and D. J. Hansen are Biologists at Bechtel Nevada, MS

NLV081, P.O. Box 98521, Las Vegas, NV 89193-8521.

Biodiversity Analysis of Vegetation

on the Nevada Test Site

W. K. Ostler

D. J. Hansen 

Abstract—The Nevada Test Site (NTS) located in south-central

Nevada encompasses approximately 3,567 km2 and straddles two

major North American deserts, Mojave and Great Basin. Transitional areas between the two desert types have been created by

gradients in elevation, precipitation, temperature, and soils. From

1996 to 1998, more than 1,500 ecological landform units were

sampled at the NTS for numerous biotic and abiotic parameters.

These data provide a basis for spatial evaluations of biodiversity

over landscape scales at the NTS. Species diversity maps (species

richness versus species abundance) have been produced. Differences in ecosystem diversity at the ecoregion, alliance, association,

and ecological landform unit levels are presented. Spatial distribution maps of species presence and abundance provide evidence of

where transition zones occur and the resulting impact on biodiversity. The influences of abiotic factors (elevation, soil, precipitation)

and anthropogenic disturbance on biodiversity are assessed.

Introduction ____________________

The Nevada Test Site (NTS) is located in Nye County in

south-central Nevada and encompasses 3,567 km2 (1,375

mi2

). Three large valleys dominate the southern two-thirds

of the NTS: Yucca, Frenchman, and Jackass Flats (fig. 1).

Mountains, mesas, and hills enclose these valleys.

During years of high precipitation, surface water collects

and forms shallow lakes in the closed basins of Yucca and

Frenchman Flats. Jackass Flats is an open basin and drains

to the southwest via Fortymile Wash. Mercury, Rock,

Topopah, and Mid valleys are smaller basins and also have

drainage outlets. Pahute Mesa and Timber and Shoshone

mountains dominate the northern, northwestern, and westcentral sections of the NTS. Elevation on the NTS ranges

from less than 1,000 m (3,281 ft) above sea level in Frenchman Flat and Jackass Flats to about 2,340 m (7,677 ft) on

Rainier Mesa. Elevations at the base of mountains on the

NTS are an average of 975 m (3,200 ft) in the south, 1,370 m

(4,496 ft) in the central region, and 1,600 m (5,250 ft) in the

northern part of the NTS. Mountains range from 1,400 to

1,800 m (4,593 to 5,906 ft) in the south and 2,100 to 2,300 m

(6,890 to 7,546 ft) in the north. Associated with these

elevation increases is the northern boundary of the Mojave

Desert and the southern boundary of the Great Basin Desert

within a broad east-west corridor of transition (Beatley

1976).

The Nevada Test Site has a climate characteristic of high

deserts with little precipitation, very hot summers, mild

winters, and large diurnal temperature ranges. Monthly

average temperatures on the NTS range from 7 °C (45 °F) in

January to 32 °C (90 °F) in July (U.S. Department of Energy

1996a). The average annual precipitation on the NTS

ranges from 15 cm (6 inches) at the lower elevations to 23 cm

(9 inches) at the higher elevations. About 60 percent of this

precipitation occurs from September through March. Winter precipitation frequently occurs as snow, which persists

in northern Yucca Flat and to the north. Higher mountains

commonly are snow covered much of the winter. Snow

seldom persists for more than a few hours in the southern

valleys.

Although the NTS was used for nuclear testing from 1951

to 1992 only about 7 percent of the site has been disturbed

(U.S. Department of Energy 1996a). Despite drastic changes

to localized areas due to nuclear testing, biological resources

over much of the NTS remain relatively pristine and undisturbed. The abuses of overgrazing by livestock, land degradation due to uncontrolled recreational uses, industrial

pollution, and other disturbances common to public lands

have been minor or absent on the NTS. Protection of its

biological resources has been strengthened by U.S. Department of Energy Policy 430.1 (U.S. Department of Energy

1996b), which mandated that land management practices

incorporate ecosystem management principles. The U.S.

Department of Energy is also working to preserve viable

populations of native plants and animals as stated in its

Resource Management Plan for the NTS (U.S. Department

of Energy 1998).

Before resources can be effectively managed and preserved, they must first be identified and described. Vegetation classification and mapping are among the first steps in

implementing ecosystem management on the NTS. Inventories and spatial mapping are useful tools to ensure that

sensitive species and habitats including areas of high biodiversity are adequately described, located, and protected.

Methods _______________________

The description of the methods used in delineating Ecological Landform Units (ELU) and gathering field data that

was used in this analysis was reported previously in early

proceedings of the Shrub Research Consortium (Ostler and

others 1999). Methods presented here describe how field

data were analyzed to obtain species diversity values and

distribution patterns.

A total of 1,508 ELUs were sampled on the NTS. At each

ELU, we obtained a list of total species observed. From this
USDA Forest Service Proceedings RMRS-P-21. 2001 239

Biodiversity Analysis of Vegetation on the Nevada Test Site Ostler and Hansen

Figure 1—Major topographic features of the Nevada Test Site.
240 USDA Forest Service Proceedings RMRS-P-21. 2001

Ostler and Hansen Biodiversity Analysis of Vegetation on the Nevada Test Site

we calculated a species richness value for each ELU. We

gathered relative abundance of woody species at each ELU

along a 200-m transect. From that abundance data, we

calculated species abundance using the Berger-Parker indices for each ELU (Berger and Parker 1970).

Based on our vegetation classification, 10 vegetation alliances and 20 associations were recognized as occurring on

the NTS (Ostler and others 2000). Alliance and associations

are described based on the standardized national classification system described by Grossman and others (1998). Species richness and species abundance were calculated for

each association and alliance. Species richness was determined by recording all unique species in each ELU. Species

richness for associations, alliances, and ecoregions were

obtained by averaging of the species richness values for

every ELU within that association, alliance, or ecoregion.

Species abundance was obtained by averaging the species

abundance values obtained for every ELU within that association, alliance, or ecoregion.

Two major ecoregions, Mojave Desert and Great Basin

Desert, can be identified from the vegetation classification of

the NTS. Between these two deserts is a broad transition

zone that often includes a mixture of species from either

major ecoregion. Beatley (1976) refers to this climatic zone

as the “Transition Desert” and recognized several plant

associations within this zone. We evaluated ecosystem diversity within these three major areas. Comparisons of species

richness and species abundance were made for each ecoregion.

There are three alliances within the Mojave Desert, three

within the transition zone, and four within the Great Basin

Desert. In terms of total area, the Great Basin Desert

occupies approximately 40 percent of the NTS, followed by

the transition zone with 37 percent. The Mojave Desert

occupies the southern 22 percent of the NTS. Sampling

within each major zone was rather even with the average

areas per ELU being 216 ha in the Mojave Desert, 221 ha in

the Transition Zone, and 233 ha in the Great Basin Desert.

Results ________________________

Species diversity has been measured by numerous methods with each method having advantages and disadvantages. The management objective of the land manager often

determines which measure of diversity should be used. Two

major types of indices, species richness and species abundance (evenness), are generally recognized in ecological

literature and these are discussed by Magurran (1988). In

this paper, we report measures for both types of indices

using two of the more commonly accepted techniques. Results of our analyses are reported at four different levels of

scale, ELU, association, alliance, and ecoregion.

Analysis at Ecological Landform Unit

Level

Species Richness—Species richness (or the number of

species) of all species encountered within each ELU is shown

in figure 2. Species richness varied tremendously across all

ELUs ranging from a low of 1 to a high of 69. The mean

species richness was 24.3 ± 10.9. The total number of species

observed across all ELUs during this study was 466. This

represents 67 percent of the total number of species (~694)

that are listed as occurring on the NTS. Most of the species

observed were forbs or grasses (~74 percent ) while shrubs

represented about 24 percent . The species richness for all of

the perennial species is shown in figure 3. The pattern of

distribution for perennial species is similar to that for all

species.

Species Abundance—The values obtained for species

abundance for the 1,508 ELUs using the Berger-Parker

index ranged from a low of 1 to a high of 6.25 (fig. 4). Four

ELUs had values of 6.25 while 11 ELUs had the second

highest values, 5.56. On the other end of the scale, 11 ELUs

had values of 1.00, meaning that a single species dominated

these sites. However, it was not always the same species that

was dominant. In those 11 ELUs with values of 1.00, seven

different species dominated at least one of the ELUs. White

burrobush (Hymenoclea salsola) dominated 3 ELUs while

fourwing saltbush (Atriplex canescens) and black sagebrush

(Artemisia nova) dominated in 2 ELUs. Basin big sagebrush

(Artemisia tridentata), shadscale (Atriplex confertifolia),

rubber rabbitbrush (Ericameria nauseosa), and blackbrush

(Coleogyne ramosissima) dominated in 1 ELU each. Most of

the ELUs (75 percent) had species abundance values under

3 while approximately 42 percent of the ELUs had species

abundance values less than 2 (fig. 4).

Analysis at Plant Association Level

Species Richness—Of the 20 plant associations recognized on the NTS, species richness ranged from a low of 13.0

in the Atriplex confertifolia-Kochia americana shrubland to

a high of 38.6 in the Artemisia nova-Artemisia tridentata

shrubland (table 1). The range of richness values among

ELUs within each association was very high. Those sites

that had poor or harsh soils or that had been subject to

previous disturbance such as in Yucca Flats tended to have

low species richness. There also appears to be a positive

relationship of species richness at the association level with

elevation and precipitation.

Species Abundance—The Berger-Parker values for associations ranged from a low of 1.62 in the Artemisia novaChrysothamnus viscidiflorus shrubland to a high of 4.03 in

the Menodora spinescens-Ephedra nevadensis shrubland.

Values for all associations are reported in table 1. The

species abundance of associations does show that transition

associations tend to have higher species abundance than

Mojave or Great Basin associations with the exception of

the Coleogyne ramosissima-Ephedra nevadensis shrubland.

Statistical analysis showed that there is no significant

correlation between species richness and species abundance

on an association level (r2 = 0.15).

Analysis at Plant Alliance Level

Species Richness—Species richness values ranged from

a low of 15.8 in the Atriplex spp. shrubland to a high of 33.7

in the Pinus monophylla/Artemisia spp. woodland alliance.

Species richness values for all associations are reported in

table 2. Those alliances that have less favorable soil conditions (Lycium shockleyi-Lycium pallidum shrubland alliance, Atriplex spp. shrubland alliance) or that have been
USDA Forest Service Proceedings RMRS-P-21. 2001 241

Biodiversity Analysis of Vegetation on the Nevada Test Site Ostler and Hansen

Figure 2—Species richness of all species for ELUs on the Nevada Test Site.
242 USDA Forest Service Proceedings RMRS-P-21. 2001

Ostler and Hansen Biodiversity Analysis of Vegetation on the Nevada Test Site

Figure 3—Species richness of perennial species for ELUs on the Nevada Test Site.
USDA Forest Service Proceedings RMRS-P-21. 2001 243

Biodiversity Analysis of Vegetation on the Nevada Test Site Ostler and Hansen

Figure 4—Species abundance using the Berger-Parker index for ELUs on the Nevada Test Site.
244 USDA Forest Service Proceedings RMRS-P-21. 2001

Ostler and Hansen Biodiversity Analysis of Vegetation on the Nevada Test Site

disturbed routinely (Hymenoclea-Lycium shrubland alliance) tend to have both lower species richness and species

abundance.

Species Abundance—The Berger-Parker values for alliances ranged from a low of 1.87 in the Atriplex spp.

shrubland alliance to a high of 3.37 in the Ephedra nevadensis

shrubland alliance. The Ephedra nevadensis shrubland alliance contains the top four associations in terms of species

abundance. Values for all alliances are reported in table 2.

Analysis at Ecoregion Level

Species Richness—Species richness was greatest in the

Great Basin Desert ecoregion. This ecoregion had a mean of

30.1 species compared to associations in the Transition Zone

(mean of 21.9 species) and the Mojave Desert (mean of 18.9

species). Similar species diversity patterns were also observed

for all combined perennial species on the NTS (for example,

Great Basin Desert: 22.8 species per ELU, Transition Zone:

17.5 species per ELU, and Mojave Desert: 13.6 species per

ELU).

Species Abundance—the Berger-Parker index showed

that unlike species richness the Mojave Desert ecoregion

had the highest species abundance with an average value of

2.67. This was followed by the Transition Zone with a value

of 2.45 and the Great Basin Desert with a value of 2.15.

Analysis of Individual Species

An advantage of having data in a GIS format is that it

allows us the flexibility to spatially display any or all of the

data. We can display the distribution of a single species on

the NTS. Not only is the presence of the species noted in each

ELU, but we can display the relative abundance of the

species in each ELU of occurrence (fig. 5). This also allows

spatial analysis of congeneric species and other associated

species and can help identify those environmental parameters that separate the distribution of those species. For

example, figure 6 shows the distribution of the three species

Table 1—Species diversity for plant associations.

Species Species

Shrubland associations No. of ELUs richness abundance

Lycium shockleyi-Lycium pallidum 6 19.0 1.99

Larrea tridentata/Ambrosia dumosa 283 18.2 2.39

Atriplex confertifolia-Ambrosia dumosa 49 19.1 3.21

Lycium andersonii-Hymenoclea salsola 13 23.2 4.03

Hymenoclea salsola-Ephedra nevadensis 44 21.9 3.45

Menodora spinescens-Ephedra nevadensis 45 17.5 2.22

Krascheninnikovia lanata-Ephedra nevadensis 30 19.3 2.25

Eriogonum fasciculatum-Ephedra nevadensis 14 22.5 3.30

Ephedra nevadensis-Grayia spinosa 89 25.5 3.56

Coleogyne ramosissima-Ephedra nevadensis 323 21.2 2.03

Atriplex confertifolia-Kochia americana 19 13.9 1.80

Atriplex canescens-Krascheninnikovia lanata 38 16.7 1.91

Chrysothamnus viscidiflorus-Ephedra nevadensis 76 28.4 2.84

Ericameria nauseosa-Ephedra nevadensis 21 22.7 2.23

Ephedra viridis-Artemisia tridentata 20 36.0 3.24

Artemisia tridentata-Chrysothamnus viscidiflorus 139 29.9 1.82

Artemisia nova-Chrysothamnus viscidiflorus 103 32.3 1.62

Artemisia nova-Artemisia tridentata 30 38.6 2.85

Pinus monophylla/Artemisia novaa 78 34.3 2.84

Pinus monophylla/Artemisia tridentataa 58 33.3 1.95

aWoodland associations.

Table 2—Species diversity at the alliance level.

Alliances Species richness Species abundance

Lycium shockleyi-Lycium pallidum shrubland 19.0 1.99

Larrea tridentata/Ambrosia dumosa shrubland 18.2 2.39

Atriplex confertifolia-Ambrosia dumosa shrubland 19.1 3.21

Hymenoclea-Lycium shrubland 17.5 2.22

Ephedra nevadensis shrubland 23.2 3.37

Coleogyne ramosissima shrubland 21.2 2.03

Atriplex spp. shrubland 15.8 1.87

Chrysothamnus-Ericameria shrubland 27.2 2.71

Artemisia spp. shrubland 32.1 1.95

Pinus monophylla/Artemisia spp. woodland 33.7 2.33
USDA Forest Service Proceedings RMRS-P-21. 2001 245

Biodiversity Analysis of Vegetation on the Nevada Test Site Ostler and Hansen

Figure 5—The distribution and relative abundance of blackbrush on the Nevada Test Site.
246 USDA Forest Service Proceedings RMRS-P-21. 2001

Ostler and Hansen Biodiversity Analysis of Vegetation on the Nevada Test Site

Figure 6—The distribution of three species of yuccas on the Nevada Test Site.
USDA Forest Service Proceedings RMRS-P-21. 2001 247

Biodiversity Analysis of Vegetation on the Nevada Test Site Ostler and Hansen

Table 3—Woody species modality in each vegetation association.

No. of

Shrubland associations modal species

Lycium shockleyi-Lycium pallidum 2

Larrea tridentata/Ambrosia dumosa 3

Atriplex confertifolia-Ambrosia dumosa 11

Lycium andersonii-Hymenoclea salsola 1

Hymenoclea salsola-Ephedra nevadensis 7

Menodora spinescens-Ephedra nevadensis 12

Krascheninnikovia lanata-Ephedra nevadensis 4

Eriogonum fasciculatum-Ephedra nevadensis 3

Ephedra nevadensis-Grayia spinosa 4

Coleogyne ramosissima-Ephedra nevadensis 8

Atriplex confertifolia-Kochia americana 3

Atriplex canescens-Krascheninnikovia lanata 3

Chrysothamnus viscidiflorus-Ephedra nevadensis 6

Ericameria nauseosa-Ephedra nevadensis 6

Ephedra viridis-Artemisia tridentata 7

Artemisia tridentata-Chrysothamnus viscidiflorus 2

Artemisia nova-Chrysothamnus viscidiflorus 6

Artemisia nova-Artemisia tridentata 5

Pinus monophylla/Artemisia novaa 8

Pinus monophylla/Artemisia tridentataa 16

a

Woodland associations.

of yucca on the NTS. Mojave yucca (Yucca schidigera) is a

Mojave Desert species and only occurs in the lower and

hotter portions of the NTS. Joshua tree (Yucca brevifolia) is

a transitional species and occurs in the central portions of

the NTS while banana yucca (Yucca bacata) prefers the

higher elevations and areas of greater precipitation that are

characteristic of the Great Basin portions of the NTS.

Modality of Woody Species

A total of 117 woody species were encountered on the

transects from which relative abundance values were obtained. Each of these species was evaluated for modality, in

other words, the association that each species reached its

maximum relative abundance. Three associations, Pinus

monophylla/Artemisia tridentata woodland (16), Menodora

spinescens-Ephedra nevadensis shrubland (12) and Atriplex

confertifolia-Ambrosia dumosa shrubland (11), had a large

number of modal species (table 3). Other associations, Lycium

andersonii-Hymenoclea salsolashrubland, Lycium shockleyiLycium pallidum shrubland, and Artemisia tridentataChrysothamnus viscidiflorus shrubland had very few, 1, 2,

and 2, respectively. Four other associations had only three

modal species. The average number of modal species appeared to be independent of the number of species that

occurred within an association (compare species richness in

table 1 and table 3).

Conclusions____________________

Understanding what is meant by diversity of an area can

be very difficult because there are many measures of diversity over different spatial and temporal scales. The two

common measures of diversity, species richness and species

abundance, are not necessarily correlated as shown in this

study. When we compared diversity at an ecoregional scale,

richness and abundance appear to be inversely related. Low

species richness appears to be associated with poor soil

conditions and disturbances. Species richness appears to be

related to increased elevation and precipitation at the NTS

with those associations and alliances in the Great Basin

Desert having higher values. Species abundance does not

show this pattern. Species abundance is often greater in

transition associations (four of the top five are transitional

associations) and alliances. There are large differences in

species modality in vegetation associations; however, no

regional patterns are discernable as to their distribution.

References _____________________

Beatley, J. C. 1976. Vascular plants of the Nevada Test Site and

central-southern Nevada: ecologic and geographic distributions.

TID-26881. Energy Research and Development Administration,

Division of Biomedical and Environmental Research. 308 p.

Berger, W. H.; Parker, F. L. 1970. Diversity of planktonic Foraminifera in deep sea sediments. Science. 168: 1345–7.

Grossman, D. H.; Faber-Langendoen, D.; Weakley, A. S.; Anderson,

M.; Bourgeron, P. S.; Crawford, R.; Goodin, K.; Landaal, S.;

Metzler, K.; Patterson, K.; Pyne, M.; Reid, M.; Sneddon, L. 1998.

International classification of ecological communities: terrestrial

vegetation of the United States. Volume I. The national vegetation classification system: development, status and applications.

Arlington, VA: The Nature Conservancy.

Magurran, A. E. 1988. Ecological diversity and its measurement.

Princeton, NJ: Princeton University Press. 178 p.

Ostler, W. K.; Hansen, D. J.; Hall, D. B. 1999. The classification of

shrublands on the Nevada Test Site. In: McArthur, E. D.; Ostler,

W. K.; Wambolt, C. L., comps. Proceedings: shrubland ecotones;

August 12–14 1998; Ephraim, UT. Proceedings RMRS-P-11.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Rocky Mountain Research Station: 137–147.

Ostler, W. K.; Hansen, D. J.; Anderson, D. C.; Hall, D. B. 2000.

Classification of vegetation on the Nevada Test Site. DOE/NV/

1171-477. Las Vegas, NV: U.S. Department of Energy, Nevada

Operations Office.

U.S. Department of Energy. 1996a. Final environmental impact

statement for the Nevada Test Site and off-site locations in the

state of Nevada, Volume 1. DOE/EIS 0243. Las Vegas, NV: U.S.

Department of Energy, Nevada Operations Office: Chapters 1–9.

U.S. Department of Energy. 1996b. DOE Policy 430.1, Land and

Facility Use Planning. Washington, DC.

U.S. Department of Energy. 1998. Nevada Test Site Resource

Management Plan. DOE/NV-518. Las Vegas, NV: Nevada Operations Office.

USDA Forest Service Proceedings RMRS-P-21. 2001 5

Ecophysiology

249

USDA Forest Service Proceedings RMRS-P-21. 2001 251

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

R. S. Criddle is Adjunct Professor and L. D. Hansen is Professor,

Department of Chemistry and Biochemistry, Brigham Young University,

Provo, UT 84602. B. N. Smith is Professor, Department of Botany and

Range Sciences, Brigham Young University, Provo, UT 84602. J. N. Church

is a Ph.D. Student, University of California, Davis, CA.

Abstract—Many factors influence species range and diversity, but

temperature and temperature variability are always major global

determinants, irrespective of local constraints. On a global scale,

the ranges of many taxa have been observed to increase and their

diversity decrease with increasing latitude. On a local scale, gradients in species distribution are observable with increasing altitude.

These gradients in species distribution have not previously been

linked to physiology. In this communication, the gradients are

proposed to be a consequence of the physical laws governing energy

transduction, acting through natural selection in response to environmental temperature variability. Measurements of rates of energy production and its use in anabolic metabolism as a function of

temperature show that respiratory rates and efficiency of green

plants are closely adapted to diurnal temperature changes and

mean temperatures of the native environment. Optimization of

energy production and use by respiratory metabolism along global

gradients in temperature and temperature variability is a genome

x environment interaction, thus is a fundamental cause of the

latitudinal/altitudinal gradients of species range and diversity.

Introduction ____________________

Gradients of species range and diversity with altitude and

latitude are observed in some taxa of both endotherms and

ectotherms (in other words, organisms, including plants, in

which cellular temperature is determined by environmental

temperature). In those taxa that exhibit an increase in

species range and decrease in diversity with increasing

latitude and altitude, an as yet unidentified fundamental

mechanism linking geographical distribution, climate and

physiology may exist (Gaston 1999; Pianka 1996). This

paper develops a hypothesis that the physical laws governing energy transduction acting through natural selection in

response to environmental variability, and on a global scale,

specifically temperature variability is such a mechanism.

Application of the laws of equilibrium and non-equilibrium

Determination of Plant Growth Rate

and Growth Temperature Range From

Measurement of Physiological Parameters

R. S. Criddle

B. N. Smith

L. D. Hansen

J. N. Church

thermodynamics and kinetics to the temperature dependence of respiratory metabolism in ectotherms leads to a

prediction of range and diversity gradients in reasonable

agreement with observations, and thus is proposed as a

fundamental cause of these gradients. We show that under

certain conditions species range is proportional to, and

diversity is inversely related to, the magnitude of diurnal or

short-term temperature changes.

Previous explanations or descriptions of species distributions have been based on observations that equatoriallowland climates are more constant than climates at higher

latitudes and altitudes (Dobzhanski 1950; Klopfer 1959;

Fisher 1960; Saunders 1968; Rapoport 1975; Brown 1984;

Stevens 1989; Hallam 1994; Hanski and Gyllenberg 1997)

or on relations among species number, land area and niche

size (Wilson 1943; Preston 1948; MacArthur and Wilson

1967; Stehli and others 1969; Levinton 1982; McIntosh

1985; Rosenzweig 1995). Differences in mutation rates in

temperate versus tropical zones, faster selection due to

increased physiological rates at higher temperatures,

nonsaturation of habitats, non-equilibrium conditions, and

temporal and latitudinal gradients of light intensity have

been postulated to contribute to species diversity (Connell

1978; Hubbel 1979; Huston 1979; Rohde 1992, 1997). Water,

soil conditions, day length, symbiotic mechanisms, and so

forth, are all important determinants of the existence of a

species at any site, but local-scale environmental properties

cannot explain the global-scale patterns of species range and

diversity. Temperature is the only global-scale abiotic factor

that could determine the global-scale distributions observed

for ectotherms.

Our hypothesis may be summarized as follows. Survival

and reproduction of an individual requires the ability to

acquire and use energy and nutrients within a given environment (Harshman and others 1999). Because this ability

varies with temperature and temperature variability, a

boundary will exist somewhere along the global-scale temperature gradient, and inversely correlated global scale of

short-term temperature variability, beyond which an organism is unable to exist and another organism adapted to the

prevailing range of temperature conditions will occupy the

succeeding temperature niche. Theoretical considerations

and experimental measurements show that metabolic rates

are adapted to mean environmental temperature while

energy use efficiency is adapted to temperature variability.

Optimizing energy use (rate multiplied by efficiency) while

maximizing probability of survival of extreme temperature
252 USDA Forest Service Proceedings RMRS-P-21. 2001

Criddle,Smith, Hansen, and Church Determination of Plant Growth Rate and Growth Temperature Range From Measurement of Physiological Parameters

events thus requires that the temperature responses of

energy metabolism be matched to both the mean temperature and the short-term or diurnal range of environmental

temperature (Preston 1948). Ectotherm distribution emerges

from the requirement for maintaining near constant intracellular ATP concentration and energy charge (phosphorylation potential, Wrigglesworth 1997) as conditions change.

A fundamental assumption of the paradigm developed in

this paper is that the temperature range of adaptation is

inversely related to mean growth rate defined as the rate of

accumulation of energy in structural biomass. Thus, for

organisms in which growth rate is important for survival or

competitiveness, optimal adaptation requires adaptation

to no broader range of temperatures than necessary, although this presents major risks to survival of the individual (Stiling 1999). The growth rate compromise between

opposing needs to tolerate temperature extremes and to

maximize energy use efficiency so as to compete for available resources is reflected in the rates and efficiency of ATP

generation and use within a temperature regimen. The

short-term (hours to days) variability of temperature and

the absolute temperatures during the growth season thus

determine the optimum energy strategy for many ectotherms. However, local and historical conditions (Rohde

1997) may override full expression of ecological consequences. Thus, for example, other reasons must be sought

for the low diversity observed in some relatively constant

temperature environments (for example, high latitude

aquatic species) and in environments where scarcity of a

necessary resource (for example, water) may play a more

important role.

Because of the availability of plant experimental data and

to avoid the complications introduced by animal behavior

(for example, mobility), this paper is focused on plants.

However, the principles apply directly to growth and distribution of all aerobic, ectothermic organisms and to

homeotherms to the extent that their distributions are

determined by the distribution of ectothermic symbionts,

hosts, and food sources. The paper discusses first the response of energy metabolism to temperature, second, the

respiratory variables that must be measured to characterize

the metabolic response to temperature and temperature

variability of an individual plant or species and the relationship of respiration to growth, third, the effect of temperature

on growth rates as derived from measurements of temperature effects on respiration, and last, the predictions of the

effects of temperature and temperature variability on species ranges and diversity.

Cellular Energy Metabolism

Response to Temperature ________

Figure 1 shows the reactions of respiratory metabolism.

A fraction of substrate carbon is catabolized via oxidative

pathways to form CO2 and the energy thus obtained is used

to synthesize ATP. Some ATP and the remainder of the

substrate carbon are used for formation and maintenance

of structural biomass. The phosphatase catalyzed

reaction(s), the ADP disproportionation reaction(s), and

alternative oxidase (or uncoupling proteins, Laloi and others 1997) pathway(s) shown in figure 1 are commonly not

included in diagrams of respiratory energy metabolism as

they are viewed as “futile” or wasteful reactions, not integral parts of properly functioning energy metabolism (Stryer

1988). However, the phosphatases and alternative oxidases must be included in proper representations of respiratory metabolism as they are absolutely necessary for

controlling [ATP] and phosphorylation potential, particularly during changes in temperature or other reaction

conditions. ADP disproportionation by adenylate kinasetype reactions with equilibrium constants near 1.0 is also

necessary to buffer ATP concentration and maintain the

proper [ATP]/[ADP] ratio (Stucki 1989). The requirement

that the phosphorylation potential (in other words, the

ratio [ATP]/[ADP] [Pi]), which is directly related to the free

energy change for hydrolysis of ATP), must remain in a

narrow range has been discussed extensively by Atkinson

(1977), largely in terms of the energy charge.

Thus, equation 1 must obtain where n is the number of

moles of ATP and t is time.

(dn/dt)synthesis = (dn/dt)loss and (dn/dt)synthesis/(dn/dt)loss = 1 (1)

The static representations in figure 1 do not clearly convey

the message that relative rates of parallel pathways of the

ATP cycle, and therefore overall reaction stoichiometries

between energy production and use, change continuously

with reaction conditions (Stucki 1989; Gnaiger and Kemp

1990; Kemp and Guan 1997). The principles of energy

coupling in biological systems elucidated by Stucki’s (1989)

studies of ATP metabolism in mammalian mitochondria at

isothermal conditions also apply to intact ectotherms with

variable temperature. Thus, the energy use efficiency of

any coupled pair of reactions is defined by the ratio of Gibbs

free energies (–∆Gdriving reaction)/(∆Gdriven reaction) (Stucki 1989;

Gnaiger and Kemp 1990; Kemp and Guan 1997). The efficiency is 100 percent when this ratio = 1, but the overall rate

is zero because the system is at equilibrium. The greater the

ratio above 1, the faster the rate, but the lower the efficiency

because the excess energy from the driving reaction is lost

from the system. Thus, there is an optimum value of the ratio

at which the system can operate at the rate required to

accomplish growth and reproduction within the time constraints of the environment while maximizing the efficiency

to the range of environmental conditions.

 CATABOLISM

 CSUBSTRATE + O2 CO2

 AOX, ATP/O = 1 COX, ATP/O =3

 SUB. LEVEL PHOS.

C6H1206 ATP ADP+Pi AMP+ADP PHOSPHATASE ADENYLATE KINASE

CSUBSTRATE + N,P,K CBIOMASS

 ANABOLISM

Figure 1—Coupled metabolic energy reactions in

biomass production.
USDA Forest Service Proceedings RMRS-P-21. 2001 253

Determination of Plant Growth Rate and Growth Temperature Range From Measurement of Physiological Parameters Criddle,Smith, Hansen, and Church

Cellular growth rates can be expressed in terms of the

relative rates of ATP synthesis and its anabolic use (Kemp

1996), equation 2.

(dn/dt)synthesis = (dnG/dt) + (dnF/dt) (2)

(dnG/dt) is the rate of synthesis of that portion of ATP used

for biosynthesis reactions including maintenance, and

(dnF/dt) is the rate of synthesis of the portion of ATP used in

futile reactions. The rates (dnG/dt), (dnF/dt), and (dn/dt)synthesis

vary with temperature, including variability in the coupling of oxidative phosphorylation, in the coupling of ATP

hydrolysis to energy requiring reactions, and in the ATP

buffering reactions. Thus, the fraction of ATP used for

biosynthesis varies with temperature. The second law of

thermodynamics defines the upper limit of the efficiency of

ATP use by requiring that (dnF/dt) > 0. At the low limit of

efficiency, ATP use in biosynthesis goes to zero, in other

words, (dnF/dt) = (dn/dt)synthesis.

The driving force for evolutionary adaptation of energy

metabolism in ectothermic organisms is optimization of the

efficiency of ATP for biosynthesis within the limits of a niche

defined by the environmental variables. This suggests that

fitness for a thermal niche may be quantified by measurements of rates of ATP reactions as a function of temperature.

Respiratory CO2 and Heat

Production Are Measures of ATP

Metabolism, Metabolic Efficiency,

and Growth Rate ________________

(dn/dt)synthesis and (dnF/dt) and the temperature dependencies of these rates can be estimated from measurements

of respiratory heat and CO2 production rates. The rate of

release of Gibbs energy (dG) in the coupled processes of

catabolism and anabolism at constant pressure is described

by

dG = dw + dQ – TdS (3)

where dw, the pdV work, is negligibly small. Under steadystate conditions, dG is proportional to (dn/dt) synthesis, which

in aerobic cells is proportional to CO2 production rates

(Kemp 1996). dQ, the rate of heat dissipation, is a measure

of dnF/dt. Thus, equation 3 shows that TdS closely approximates the rate of energy accumulated in structural biomass (in other words, growth rate). Since TdS = (dG – dQ)

therefore

Growth rate = k(dnG/dt) = k [(dn/dt)synthesis – (dnF/dt)] (4)

where k is a proportionality constant. Equation 5, previously

developed by Hansen and others (1994) is equivalent to

equation 4.

RSG∆HB = –[RCO2 (1–γp/4) ∆HO2] – q (5)

RSG is the specific growth rate (mol C s–1 g–1) and ∆HB is the

enthalpy change for the reaction Csubstrate → Cbiomass (kJ mol

C–1). Therefore, RSG∆HB is specific growth rate expressed as

the rate of storage of chemical energy in structural biomass

with units of kJ s–1g–1. RCO2 is the specific CO2 production

rate (mol s–1g–1), ∆HO2 is approximately constant with a

value of –455 kJ mol–1 (Erickson 1987; Hansen and others

1997), γp is the mean chemical oxidation state of the substrate carbon, and q is the specific metabolic heat production

rate (kJ s–1 g–1).

Because ∆HB is normally positive, it follows that q/RCO2 is

a measure of efficiency, in other words,

q/RCO2 = K[(dnF/dt) / (dn/dt)synthesis] = K(1–εATP) (6)

where K is a ratio of proportionality constants relating q to

(dnF/dt) and RCO2 to (dn/dt)synthesis and εATP is efficiency of

ATP use.

Experimental measurements on many plants (and insects, fish eggs, yeast, and so forth) show that the temperature dependence of q and the temperature dependence of

RCO2, and therefore the temperature dependencies of (dnF/dt)

and (dn/dt)synthesis, differ within individuals, among individuals, within a species, and among species (Criddle and

others 1994, 1996a, 1997; Anekonda and others 1996).

Consequently, (dnF/dt)/ (dn/dt)synthesis, and q/RCO2, are functions of temperature.

Energy use efficiency can be extremely sensitive to small

differences in temperature, emphasizing the importance of

temperature in determining which organisms can survive,

compete, and reproduce in a particular niche. The efficiency

of ATP use, εATP, is not directly measurable, but is related to

the substrate carbon conversion efficiency, ε, which is also

related to q/RCO2 (Hansen and others 1994).

Temperature Dependence of Growth

Rates and Temperatures Allowing

Growth ________________________

The temperatures at which experimentally determined

temperature functions of q and (1–γp/4)455RCO2 cross define

the limits to the growth temperature range (equation 5). As

examples, figure 2 shows plots of q and 455RCO2 and RSG∆HB

versus temperature for cultivars of tomato, as a representative warm climate plant, and cabbage, as a representative

cool adapted species (Criddle and others 1997). The curves

for q are approximately Arrhenius functions over the temperature range allowing growth. RCO2 increases exponentially only up to about 20 °C (tomato) and 16 °C (cabbage). At

higher temperatures RCO2 decreases. Tomato has a larger

temperature dependence for 455RCO2 than for q over much

of the growth temperature range. The difference between

455RCO2 and q [and therefore between (dn/dt)synthesis and

(dnF/dt)] is positive only in the temperature range above 13–

14 °C and below about 37 °C. For cabbage, the temperature

dependencies of q and RCO2 are more similar, and 455RCO2 ≥ q

(in other words, RSG∆HB is positive) only at temperatures

below about 20 °C. Figure 2C shows that temperature

ranges with positive values of RSG∆HB correspond to the

growth temperature ranges for these two cultivars.

Because the temperature dependence of q is typically

greater than the temperature dependence of RCO2 in cold

adapted plants (Criddle and others 1996a,b, 1997; Anekonda

and others 1996; Hansen and others 1997; Earnshaw 1981)

efficiency of cabbage growth decreases as temperature increases and a temperature is reached where q > 455RCO2, in

other words, the temperature at which the rate of energy

production is exceeded by demands for ATP use is at the
254 USDA Forest Service Proceedings RMRS-P-21. 2001

Criddle,Smith, Hansen, and Church Determination of Plant Growth Rate and Growth Temperature Range From Measurement of Physiological Parameters

high temperature limits for these plants. At this temperature, the ATP/ADP ratio (and the phosphorylation potential)

becomes too low to drive biosynthesis, and growth stops. At

low temperature, growth rates of cold adapted plants will

slow in spite of high efficiency because of the effect of

temperature on metabolic rate.

In warm climate plants such as tomato where the temperature dependence of q ≤ the temperature dependence of

RCO2, efficiency decreases as temperature falls and the lower

temperature limit to growth occurs at the temperature at

which [(1–γp/4) 455RCO2 – q] becomes zero (Criddle and

others 1997). The high temperature decrease of tomato

growth rate shown in figure 2C results from a rapid decrease

in RCO2 that is not predicted by Arrhenius extrapolation of

data collected at lower temperatures. Because the temperature coefficient of RCO2 is greater than that for q, the rate of

ATP synthesis increases faster with increasing temperature

than the rate of ATP loss, in other words, d(dn/dt)synthesis/dT

becomes much greater than d(dnF/dt)dT, and with increasing temperature, (dnG/dt) approaches (dn/dt)synthesis. Efficiency and metabolic rate both increase and growth rate

increases. But, this can only continue to a maximum (dn/

dt)synthesis /(dnF/dt) (or 455RCO2/q) of about 1.4 (corresponding to an εATP of about 0.75). Because a large ratio of [ATP]/

[ADP] is incompatible with optimal economic growth (Stucki

1989; von Stockar and Marison 1993; Nath 1998; Ksenzhek

and Volkov 1998) as the maximum value if this ratio is

approached, the capacity of the ATP buffering enzyme systems is exceeded (Stucki 1989; Hoh and Cord-Ruwisch

1997), the ATP/ADP ratio becomes so large that the positive

∆G for ATP synthesis exceeds the negative ∆G from the

oxidation reactions, ATP synthesis and correspondingly

RCO2 is greatly reduced (as shown experimentally in fig. 2),

energy use efficiency decreases to near zero, and growth

stops.

The mean temperature and diurnal and short-term

growth seasonal range of temperatures allowing growth,

and therefore plant distribution, are thus explicitly determined by the kinetic laws of temperature dependence of

chemical reactions and the thermodynamic laws governing

energy coupled processes in changing environments. The

functioning of these laws in plants is evident from measurements of q and RCO2 and their change with temperature in many species (Hansen and others 1994; Criddle and

others 1994, 1996a,b, 1997; Anekonda and others 1996;

Hansen and others 1997). If we assume an Arrhenius temperature dependence of q and RCO2, the allowable growth

temperature range (∆T) can be calculated for various combinations of the temperature dependencies of q and RCO2,

as shown in figure 3. The temperature range over which

455RCO2/q changes from 1 (zero efficiency) to 1.4 (maximum

efficiency) is defined as ∆T. ∆T is plotted against the

Arrhenius temperature coefficient for RCO2 (μCO2) for various fixed values of the temperature coefficient of q (μq). The

region with μCO2 from approximately 3 to 11 kK and ∆T

from 5 to 37 °C includes essentially the entire physiological and environmental range. A similar set of curves could

be drawn for μq > μCO2.

Figure 3 shows how the temperature dependencies of q

and RCO2 (in other words, of (dnF/dt) and (dn/dT)synthesis,

Figure 2—The temperature dependence of respiratory

metabolism and growth rates of tomato and cabbage.

Field observations show that the cabbage cultivar grows

at low temperature, but growth ceases when the temperature is above about 20 °C. The tomato cultivar does

not grow at temperatures below about 12 °C or above

35 °C. (A) Responses of 455RCO2 (open symbols) and q

(solid symbols) values of tomato to changes in temperature. (B) Responses of the rate of CO2 production (as

455RCO2) and heat rate (q) values of cabbage to changes

in temperature. (C) Calculated values of the rates of

deposition of respiratory energy in structural biomass

(RSG∆HB) for tomato (solid symbols) and cabbage (open

symbols) across their growth temperature ranges.
USDA Forest Service Proceedings RMRS-P-21. 2001 255

Determination of Plant Growth Rate and Growth Temperature Range From Measurement of Physiological Parameters Criddle,Smith, Hansen, and Church

Figure 4 shows that the penalty associated with an

organism being adapted to a wider temperature range

than required is a decreased growth rate. Plants adapted to

a wide temperature range are capable of survival in a

climate with little temperature variation, but to the extent

that growth rate determines competitiveness, a widely

adapted plant (a temperature generalist) will be out-competed by a narrowly adapted plant (a temperature specialist). However, plants adapted to too narrow a temperature

range cannot tolerate the wide temperature range because

much of the time they would be subjected to temperatures

that disallow control of ATP metabolism.

An experimental test of the predicted inverse relation

between environmental temperature range ∆T and growth

rate has been done with 17 half-sib families of 15-year-old

Pinus ponderosa planted at three or four sites with different

latitudes and elevations (Church 2000). Plots of ∆T, the

mean diurnal temperature variation during the growth

season at each site versus height growth, show a linear

decrease in height with increasing ∆T. Linear regression

analysis of data for the 17 families gave an average regression coefficient (r2

) of 0.96 with a range from 0.88 to 0.99.

Growth rate of these trees is not correlated with any other

environmental variables except those co-correlated with ∆T.

A perfect adaptation of plants to temperature is not

possible because climates vary from year to year. Thus,

while individual plants are genetically limited in their

response to temperature, a species evolves many genotypes

with a range of responses. In addition, plants may alter their

effective environmental growth temperatures simply by

altering the time during the season when growth occurs.

There is thus no “best” solution for adaptation of energy

metabolism and growth rate to a location. Rather, plants

with a range of properties exist both within and between

species. However, the allowable ranges of energy metabolism and growth rate responses to temperature must change

systematically with diurnal temperature range. Because of

the covariance between diurnal temperature range ∆T and

latitude/altitude, the relations among temperature, energy

Figure 3—Dependence of the range of temperatures allowing growth (∆T) on values of the Arrhenius

temperature dependence of q and RCO2 (μq and μCO2).

(A) Each curve represents ∆T dependence on μCO2 at

a different, constant μq. The μq values plotted are μq =

1.2 (open circles), μq = 1.5 (filled squares), μq = 2.0

(filled triangles), and μq = 2.5 (filled diamonds). The

box insert includes the total range of experimentally

observed combinations of μq and μCO2.

respectively) determine fitness for a particular climate. If

∆Tclimate > ∆T (μCO2 – μq) of the plant, the plant will not thrive

if it spends too much time at the extreme temperatures

where efficiency is zero. If ∆Tclimate < ∆T (μCO2 – μq) of the

plant, the plant will be less competitive than plants with

∆T(μCO2 – μq) closer to ∆Tclimate. The minimum ∆T of about

5 °C is obtained only at large values of (μCO2 – μq). The

maximum and minimum values of (μCO2 – μq) measured in

our laboratories on ectotherms are about plus or minus 6 kK,

(or a difference in Q10 values for RCO2 and q of about 2.0).

When the absolute value of (μCO2 – μq) is less than about 0.8

kK, ∆T reaches 32 to 37 °C and growth is possible in

extremely variable climates, but efficiency for converting

photosynthate into structural biomass is very low.

Figure 4 shows a three-dimensional model of the relations

among growth rate (as RSG∆HB), the ratio of temperature

coefficients μq/μCO2 (varied from 1:2 to 2:1), and temperature

from 0 to 40 °C, derived from experimental data on maize

(Taylor and others 1998, and unpublished data). High growth

rates are obtained when the ratio μq/μCO2 is either very large

or very small. When μq >> μCO2, the growth temperature

range is small and growth rate maxima occur at low temperatures. When μq ≈ μCO2, growth temperature range is

large, but growth rate is small across the entire range. (In

the limit where μq = μCO2 , the temperature range is infinite,

but growth rate is zero.) When μCO2 >> μq, the growth

temperature range is again small, but growth rate maxima

occur at high temperature. Growth rate reaches a maximum

where 455RCO2/q = 1.4 and rapidly declines with further

increase in temperature. The higher the ratio μCO2/μq, the

lower the temperature at which the optimum is obtained.

The projected contour map at the top of figure 4 allows

visualization of the decrease of growth rate at temperatures

above optimum.

0.5

0.7

0.9

1.1

1.3

μq/μ 0

CO2

8

16

24

32

TEMPERATURE, oC

0

0

1

1

2

2

3

3

4

4

5

5

RSG∆HB

RSG∆HB

Figure 4—Growth rates for maize as a function of

temperature and the ratio μCO2/μq calculated from data

on maize cultivars.
256 USDA Forest Service Proceedings RMRS-P-21. 2001

Criddle,Smith, Hansen, and Church Determination of Plant Growth Rate and Growth Temperature Range From Measurement of Physiological Parameters

use efficiency, and growth rate are a fundamental mechanism that may explain the observed latitudinal and altitudinal gradients of species range and diversity.

The relation between climate and respiration has been

further tested with three Eucalyptus species from different

native climates with approximately the same mean temperature, 16.4 °C, but different temperature variation ∆T.

Plots of RSG∆HB versus temperature for individual trees of

each species, grown in, and therefore acclimated to, a common environment, are presented in figure 5. Differences

between species are much larger than intra-species variation and the patterns shown are representative of the species. Because these species grow throughout the year, annual temperature data describe the growth temperature

range. The native environmental temperature ranges are

similar to, and give the same ranking of ∆T as the temperature range of positive values of RSG∆HB, which were calculated from measured q and RCO2 values (equation 5 with γ =

0). Acclimation of the trees to climate in the common growth

environment is negligible because the temperature ranges

allowing growth (positive RSG∆HB) are the same as the

climatic temperature ranges at the different growth sites.

Predicted Magnitudes of Gradients

of Species Range and Diversity____

The principles developed above predict that range or niche

size for growth of individual populations and species must

increase with the magnitude of temperature fluctuations

(∆T) (equation 8)

AT /NT = c (∆T) (8)

where AT is total area, NT is total number of species, and AT/NT

is the average species area. c is a proportionality coefficient.

∆T is related to latitude and altitude, in other words, ∆T = c’

f(latitude, altitude). Through mid-range temperate latitudes

and altitudes, the relation between ∆T and latitude or altitude

is approximately linear so that in this range, species area,

latitude/altitude, and ∆T are nearly linearly related.

Consider the effects of this relation on species areas in the

northern hemisphere from 12° to 45° north latitude. The

approximate mean temperature fluctuation (∆T) at 45°

latitude is about 3 times that at 12° latitude. Thus, the niche

size increases (and number of thermal niches decreases)

about threefold from 12 to 45°. However, if areas at the two

latitudes are not constant, then the effect of area on species

numbers also enters in.

An exponential relation exists between species number

(N) and area (A), in other words, N = kAz

. z values from 0.1

to 0.6 have been reported (Rosenzweig 1998). For example,

Hanski and Gyllenberg (1997) showed (for moth species)

that plots of ln N versus ln A (of islands in an archipelago)

yielded a line with slope, (or z value) near 0.4. Using this

value and returning to our example, we find that the land

area of the continents increases about 1.5 fold from 12° to 45°

north latitude. The species area relation predicts N should

be (1.5)0.4 = 1.2 fold higher at 45°, a trend in species diversity

opposite that observed. However, combination of the species

area relation with equation 8 and the effects of latitude on

species range yields equation 9,

N[(1/z) – 1) = c’’ ∆T (9)

where c’’ is again a constant. Comparison of species numbers at 12 °C and 45 °C north latitude using the combined

temperature and area gradient effects indicates a decrease

in number of species per unit area by a factor of 2.08.

Species diversity should thus decrease about twofold from

12° to 45° north latitude, which agrees reasonably well

with relative values noted for species diversities at these

latitudes (Rohde 1997).

The concept that temperature dependence of cellular energy production by respiration contributes to the gradient of

species diversity thus predicts the correct direction and allows an a priori estimation of the magnitude of the temperature-linked portion of the gradient of species diversity with

latitude and altitude. It should be noted that there is no clear

test of this number available in the literature. All studies to

date examined limited areas where local climatic and geographical factors play important determinant roles in range

and species numbers. Because ∆T is a function of latitude/

altitude, the apparent value of the exponent, z, in species area

curves will not be constant, but will increase with increasing

latitude and altitude. This probably accounts for much of the

observed variation between studies in values of z (Rosenzweig

1998).

Figure 5—Growth rates of plants from three Eucalyptus

species calculated as a function of temperature from q and

RCO2 measurements and comparison with temperature

ranges at the native growth sites of E. Saligna (Smith), E.

grandis (W. Hill ex Maiden), and E. globulus (Labill. subsp.

maidenii {F. Muell} Kirkpatr., commonly known as E.

Maidenii) (Boland and others 1984). The trees tested were

seedlings grown hydroponically in a common, controlled

environment chamber. Measurements of q and RCO2 were

made at several temperatures on small, expanding leaf

tissues, followed by calculation of growth rates, RSG∆HB,

by equation 8 with γ = 0 (Hansen and others1994). Lines

at the lower portion of the figure connect the mean high

temperature of the warmest month and the mean low of the

coldest month at each site.

globulus

grandis

saligna

globulus

saligna

grandis

Native temperature range

Temperature, °C
USDA Forest Service Proceedings RMRS-P-21. 2001 257

Determination of Plant Growth Rate and Growth Temperature Range From Measurement of Physiological Parameters Criddle,Smith, Hansen, and Church

Because optimization of metabolic properties with temperature within species must follow the same rules as for

species, gradients of responses to temperature must exist

within species. This intra-species variability helps ensure

species survival during climate changes or influxes of competitors and provides the opportunity for farmers and plant

scientists to select the best genotypes for optimal growth at

a given site. These principles provide a unifying rationale for

improving production by matching cultivars to environment. This paper has focused on plants, but the principles

are applicable to ectothermic animals. Also, questions of

ectotherm responses to climate change can be framed in

more quantitative terms with an understanding of the

underlying causes.

Summary ______________________

We conclude that the temperature responses of cellular

energy metabolism are a fundamental determinant of

latitudinal/altitudinal gradients of species range and diversity. To maximize the probability of growth, reproduction,

and survival, organisms have been selected to optimize their

ability to obtain and use energy throughout the range of

ambient temperatures. Matching energy metabolism to climatic temperature is accomplished by variable engagement

of “futile” reactions that are necessary to maintain efficient

energy coupling with changing temperatures. Ectotherms

growing in climates with a narrow temperature range can

evolve high energy use efficiencies and enhance their ability

to compete for resources, but in doing so they risk being

damaged or killed by temperature excursions outside the

normal range. Ectotherm adaptation to broad temperature

ranges enhances survival during extreme temperature excursions, but at the cost of lower growth rates. Energy

efficiency and survival requirements lead to species variability along latitudinal and elevational gradients of temperature range and diversity.

Acknowledgments ______________

The authors appreciate support for this work from

Simpson Timber Co., The Northern Sierra Tree Improvement Association, and from BYU. Support was obtained

from C.N.R.S. by L.D.H. during a stay at the Laboratorie de

Thermodynamique et Genie Chimique, Universite Blaise

Pascal, Clermont-Ferrand, France, while on leave from

BYU. RSC gratefully acknowledges support from the Lady

Davis Fellowship Trust for a visit at Hebrew University in

Rehovot during development of this manuscript.

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USDA Forest Service Proceedings RMRS-P-21. 2001 259

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Richard S. Criddle is an Adjunct Professor and Lee D. Hansen is a

Professor, Department of Chemistry and Biochemistry, Provo, UT 84602.

Bruce N. Smith is a Professor, Department of Botany and Range Sciences,

Brigham Young University, Provo UT 84602. J. N. Church is a Ph.D. Student,

University of California, Davis, CA.

Abstract—The Arrhenius activation energies, and therefore temperature coefficients, for rates of catabolic production of ATP and for

anabolic use of ATP differ. Because the intracellular concentration

of ATP and the phosphorylation potential must be controlled within

a narrow range for cell survival, a mechanism must exist to balance

these rates during temperature variation in ectotherms. We hypothesize that much of this control is accomplished via engagement

of temperature-dependent reactions that waste ATP or the potential to make ATP in “futile” cycles and that energy-wasting metabolic cycles are essential for maintaining acceptable phosphorylation potentials across a temperature range. We further postulate

that the mitochondrial alternative oxidase (AOX) activity is one

important mechanism for “wasting” potential to make ATP and thus

for controlling the phosphorylation potential in plants as temperature or other reaction conditions vary. Because of differences in

temperature coefficients, the ratio of AOX to COX activities varies

with temperature, resulting in a temperature-dependent change in

coupling oxidation to phosphorylation. Matching the changes in

substrate carbon conversion efficiency to environmental temperature patterns allows plants to maintain constant phosphorylation

potentials. Thus, an apparent paradox exists that survival of all organisms in changing conditions depends on an energy loss via “futile

cycles.”

The Need for Futile Cycles ________

The biological function of apparently “futile” reactions has

long been a subject of speculation. What is the purpose of the

ubiquitous reactions that lose energy by cyclic production

and breakdown of reaction intermediates or via reactions

that result in energy loss by short-circuiting the formation of ATP? The answer to this question is known only for

futile reactions employed in specialized thermogenic tissues. “Futile” reactions must contribute positively to fitness

in non-thermogenic tissues or they would have been eliminated by natural selection. This study examines the hypothesis that an uncoupled energy loss is required to maintain

Responses of Plant Growth and Metabolism

to Environmental Variables Predicted From

Laboratory Measurements

Lee D. Hansen

Bruce N. Smith

Richard S. Criddle

J. N. Church

[ATP] and phosphorylation potential nearly constant in

varying cellular conditions and is therefore particularly

important for survival of ectotherms in variable temperature environments.

The overall reaction for aerobic growth of plants may be

written as in equation 1.

Csubstrate + x(compounds and ions of N, P, K, etc.) +

yO2 → ε Cstructural biomass +(1-ε)CO2 (1)

Reaction 1 is the sum of two reactions, the catabolic reaction (2)

Csubstrate + yO2 + nADP + nPi + aNAD+ → CO2 +

nATP + aNADH + aH+ (2)

And the anabolic reaction 3.

Csubstrate + x(compounds and ions of N, P, K, etc.) +

mATP + bNADH + bH+ →

Cstructural biomass + mADP + mPi + bNAD+ (3)

Reactions 2 and 3 occur in the condition-dependent ratio

(1- ε)/ε where ε is the substrate carbon conversion efficiency.

Reactions 2 and 3 are energy-coupled through cyclic production and hydrolysis of ATP and redox cycling of NADH.

Because the rates of reactions 2 and 3 have different dependencies on temperature and other conditions, the coefficients n and m, and a and b, are generally not equal for the

two reactions. Principles of nonequilibrium thermodynamics

applied to the energy-coupled system of reactions 1–3 lead to

the conclusion that reaction 2 must always produce ATP and

NADH at rates equal to or in excess of their rates of use in

the biosynthetic reactions of reaction 3 (in other words, n ≥

m and a ≥ b). If ATP is synthesized faster than it is used for

biosynthesis, the excess can be disposed of by hydrolytic

reactions, but if ATP is synthesized slower than it is used,

the phosphorylation potential, or free energy change for

hydrolysis of ATP (∆GP, Equation 4), falls and cell death

ensues. Therefore, the excess ATP and NADH is cycled

through condition-dependent uncoupled hydrolysis and oxidation reactions in order to maintain the phosphorylation

potential and [ATP] approximately constant.

∆Gp = -RTln [ATP]/[ADP][Pi] ≈ constant (4)

The rate of synthesis of ATP is also controlled by conditiondependent reactions that cause a loss of the potential to form

ATP, in other words, reactions mediated by uncouplers and

through such pathways as the alternative oxidase. The

engagement of these less efficient alternate pathways of

oxidation to control [ATP] and phosphorylation potential
260 USDA Forest Service Proceedings RMRS-P-21. 2001

Hansen, Smith, Criddle, and Church Responses of Plant Growth and Metabolism to Environmental Variables Predicted From Laboratory Measurements

varies with reaction conditions. This variation is independent

of the rate of reaction 3 because reactions 2 and 3 are not

closely coupled. The overall result is a condition-dependent

energy loss and a variable efficiency of energy coupling

between catabolic and anabolic processes (Wrigglesworth

1997).

The requirement demonstrated above for engagement of

less efficient pathways in plants to maintain phosphorylation potentials under variable reaction conditions is also

apparent from fundamental thermodynamic considerations.

The second law of thermodynamics requires that mass and

energy flow through the system (described by equation 1)

must be accompanied by an entropy increase, in other words,

processes such as growth require a transfer of energy from

the system to the surroundings. This is measurable as heat

loss to the environment (Jou and Llebot 1990). When the

reactions occur at steady state, the entropy (heat) loss to the

surroundings is minimized (Prigogine 1980). Any displacement from steady state, in other words, varied reaction

conditions, results in an increased energy loss to the environment. Various workers (Jou and Llebot 1990, p. 51) have

confirmed that these concepts apply to growth of cells under

near steady state conditions and have used measurements

of heat dissipated as an indication of the increase in entropy

during variable growth conditions. We propose that the

concepts also apply to rapidly growing plant tissues with

adequate substrate supplies. Thus, variation in reaction

conditions that perturb steady-state growth (or further

displace a growing system from steady state) results in an

experimentally measurable increase in heat loss and an

overall decrease in energy use efficiency during growth.

Several sources infer (but do not rigorously prove for biological systems) that the larger and more frequent the variations perturbing steady-state growth, the greater the energy

loss from the system (Zotin 1990; Lewis and Randall 1961,

unpublished observations by the authors).

Futile Reactions in Plant

Metabolism ____________________

Thermodynamic arguments clearly require variable efficiency and increased heat loss with variable growth conditions. However, the mechanisms by which energy is lost and

mechanisms by which the energy loss and changing efficiency are matched to environmental conditions to ensure

optimal growth and survival are not defined by the thermodynamic arguments. The mechanisms may be derived from

analysis of the effects of changing conditions on enzyme

activities involved in intracellular ATP energy cycles.

The ATP cycle for aerobic cellular energy metabolism may

be presented in the form of two half-cycles, the catabolic

formation of ATP and the anabolic hydrolysis and use of ATP

(Kemp 1996) (fig. 1).

The concentrations of adenine nucleotides in cells is low (a

few mM) and the rate of turnover of ATP is high (up to 1 g

ATP per g rapidly expanding plant tissue per day). Thus,

rates of the two halves of the cycle in figure 1 must remain

carefully balanced to maintain [ATP] constant and the

phosphorylation potential in the narrow range required for

cell viability (Kemp 1996). However, variation in reaction

conditions cause changes in the relative rates of all the

reactions involved in ATP synthesis and breakdown. Because

all cells experience changing reaction conditions during

growth, all must have mechanisms to control the rates of

synthesis and breakdown of ATP and the phosphorylation

potentials. Such controls have frequently been discussed in

terms of energy charge, with emphasis on regulation by

adenylate binding to glycolytic enzymes (Atkinson 1977).

However, simple feedback inhibition/activation by intermediates in energy metabolism alters rates, but not stoichiometry, and does not facilitate the thermodynamically

required changes in stoichiometry and efficiency required

during changes in reaction conditions. Multiple, parallel

reactions with different effects on energy coupling as shown

in figure 1 provide control of phosphorylation potential by

altering the energy coupling efficiency.

Homeotherms, which experience relatively small changes

in reaction conditions, contain enzymes or enzyme systems

such as phosphatases and uncoupling proteins to control

phosphorylation potentials during changing reaction conditions (Stucki 1989; Nath 1998). Ectotherms face a major

additional problem in maintaining phosphorylation potentials during temperature change and require these enzymes

plus enzymes that can adjust metabolic responses to the

large temperature change. This becomes particularly evident from observations that the Arrhenius activation energies, and therefore the temperature dependencies of the

rates of ATP synthesis and its anabolic use, are not the same

(Criddle and others 1997; Taylor and others 1998; Smith and

others 1999). Therefore, in the absence of a regulatory

mechanism the relative rates of catabolic formation of ATP

and its use in anabolic reactions would change continuously

with changing temperature and [ATP] would vary with

temperature. Ectotherm survival thus requires mechanisms

to facilitate varying catabolic/anabolic stoichiometries, control phosphorylation potential and optimize energy use

efficiency over a broad temperature range.

Some enzyme reactions that can function to control phosphorylation potential or alter the stoichiometries of oxidative phosphorylation and anabolic use of ATP for production

of biomass are shown in figure 1 (reactions indicated with

Figure 1—ATP cycle for plant respiration and

biomass synthesis.

 CATABOLISM

 CSUBSTRATE + O2 CO2

 AOX, ATP/O = 1 COX, ATP/O =3

 SUB. LEVEL PHOS.

C6H1206 ATP ADP+Pi AMP+ADP PHOSPHATASE ADENYLATE KINASE

CSUBSTRATE + N,P,K CBIOMASS

 ANABOLISM
USDA Forest Service Proceedings RMRS-P-21. 2001 261

Responses of Plant Growth and Metabolism to Environmental Variables Predicted From Laboratory Measurements Hansen, Smith, Criddle, and Church

dashed arrows). For example, variation in relative amounts

of substrate level phosphorylation can alter the ratios of

substrate level to oxidative phosphorylation and affect overall reaction stoichiometries and energy use efficiency. The

adenylate kinase reaction plays a critical role in buffering

phosphorylation potentials against small changes in reaction conditions or intermediate concentrations (Stucki

1989). Phosphatases can alter energy-coupling stoichiometries via a classical “futile cycle” hydrolysis of ATP without

accomplishing biochemical work. Uncouplers or uncoupling

proteins can also cause a “futile” energy loss. However, this

group of reactions probably plays a relatively limited role in

balancing the overall condition-dependent production and

use of ATP during metabolism of healthy, aerobic plant cells.

In contrast, because it is often present with high and

variable activity in plant cells, the mitochondrial alternative oxidase (AOX) can have large effects on the efficiency

of coupling energy metabolism to biomass production. Substrate oxidation via COX yields a maximum of 3 ATP mol-1 O2.

The alternative oxidase enzyme has no phosphorylation

site and oxidation via the AOX pathway yields a maximum

of 1 ATP mol-1 O2. Oxidative energy that could have been

used to synthesize two additional ATP is lost as heat.

The AOX catalyzed reaction thus causes a “futile” energy

loss. Consequently the number of moles of substrate required to produce one mole of ATP depends on the AOX/

COX ratio (Lance and others 1985). Because the temperature coefficients of AOX and COX are not the same (McCaig

and Hill 1977; Smakman and others 1982; Purvis 1985;

Mc Nultly and Cummins 1987), this ratio changes with

temperature (and probably with other reaction conditions).

Figure 1 illustrates how changing this ratio changes the

substrate carbon conversion efficiency, ε (in other words,

the fraction of substrate carbon incorporated into structural biomass).

Thus, we hypothesize that the “futile” waste of the potential to produce ATP and the futile hydrolysis of ATP are the

mechanisms by which phosphorylation potentials are controlled in plants growing in a variable temperature environment. We further propose that a primary reaction for adjusting the efficiency of ATP synthesis and maintaining the

near constant phosphorylation potential in plants is the

mitochondrial alternative oxidase. The relative temperature coefficients of the AOX and COX reactions determine

the rate of change in efficiency with temperature and thereby

the fitness of a plant for growth in a particular temperature

environment. Matching a plant to environmental temperature is achieved by balancing the temperature coefficients of

ATP synthesis, ATP use in anabolic reactions and ATP (or

the potential to make ATP) wasted so that energy use

efficiency is optimized over the time-temperature distribution during the growth season.

A quantitative test of these hypotheses is possible by

comparison of data from direct calorespirometric measurements of substrate carbon conversion efficiencies of many

different plants (Criddle and others 1997; Taylor and others

1998; Smith and others 1999) with measurements by

Gonzalez-Meler and others (1999) of AOX and COX reaction

rates of soybean and mung bean at 14 and 28 °C.

Demonstration of Futile Cycle

Function From Changes in

Substrate Carbon Conversion

Efficiency With Temperature ______

Substrate carbon conversion efficiencies of plants can be

calculated from direct calorimetric measurements of rate of

heat loss (q) and either the CO2 production rate (RCO2) or the

rate of O2 consumption (RO2) for rapidly growing plant

tissues. The ratio of heat loss per mole CO2 produced (or O2

consumed) is a direct, and intuitive, measure of efficiency.

The more heat lost per C-mole respired to CO2, the less

efficient the transfer of respiratory energy into anabolic

products. The relation between q/RCO2 and ε is shown in

equation 5 (Hansen and others 1994)

q/RCO2 = -(1-γp/4) ∆HO2 –[ε/(1-ε)]∆HB (5)

where γp is the chemical oxidation state of the stored photosynthetic products used as substrate for biomass production, ∆HO2 = -455 kJ mole-1, and ∆HB is the enthalpy of

incorporation of C into biomass, as kJ mole-1 C. As q/RCO2

increases, ε decreases (so long as the chemical nature of the

photosynthetic substrate and biomass remain constant).

Simultaneous measurement of q and RCO2 on rapidly

growing seedling tissues of cold climate plants, such as

maize cultivars adapted for cultivation in the northeastern

U.S. and eastern Canada, show increasing q/RCO2 as temperature increases (Criddle and others 1997; Taylor and

others 1998) (table 1). Thus, ε for these plants decreases

with increasing temperature. For example, an increase in

Table 1—Measured changes in q/RCO2 with temperature and calculated substrate carbon conversion efficiency.

q/RCO2, kJ mol–1 ε, percenta

14 °C 28 °C 14 °C 28 °C

Maize cultivarb

G17 (cool climate) 250 425 67 56

814 (warm climate) 400 295 44 60

T10 (cool climate) 225 425 70 23

Tom Thumb (warm) 444 338 10 54

Other species q/RCO2

Cool climate 14 °C 28 °C

Eucalyptus globulus 245 >700

Cabbage 310 >800

Strawberry 320 500

Cheat Grass 328 455

Warm climate

Eucalyptus grandis 414 347

Tomato 425 375

Lily 305 255

Rice (Italico livorno) 404 345

a

Calculations of ε with equation 5 used measured values of q and RCO2 and the

assumption that ∆HB = 100 kJ mol–1 C incorporated into plant biomass, with

carbohydrate as the substrate carbon source, in other words, γp = 0. b

Data from (Taylor and others 1998).
262 USDA Forest Service Proceedings RMRS-P-21. 2001

Hansen, Smith, Criddle, and Church Responses of Plant Growth and Metabolism to Environmental Variables Predicted From Laboratory Measurements

temperature from 14 to 28 °C caused an increase in q/RCO2

from about 250 to 425 kJ mol-1 in the cold-climate adapted

Pioneer Seed maize cultivar G-17. This corresponds to a

decrease in ε from 67 to 56 percent. In contrast, there is a

decrease in q/RCO2 from about 400 to 295 kJ mol-1 when

temperature is increased from 14 to 28 °C for the warmer

climate adapted Pioneer Seed maize cultivar 814. This

corresponds to an increase in efficiency of seedlings from

about 44 to 60 percent over this range (table 1). Values for

additional maize cultivars and other species are included in

table 1 to show that changes in q/RCO2 and ε for maize

represent common trends for warm and cool climate plants

(Smith and others 1999; Criddle and Hansen 1999). Thus,

simple experimental measurements on plant tissues quantify values of ε and show that ε changes systematically with

temperature in a pattern specific to growth temperature

conditions.

Warm climate cultivars commonly increased while ε of

the cooler climate cultivars decreased with increasing

temperatures in the range studied (table 1). Since thermodynamic considerations require that efficiency must change

with temperature, it is not unexpected that each species or

cultivar is adapted to have higher efficiency in the temperature range to which it is adapted. Note that the designation

of warm and cool climates refers to temperatures experienced during the growth season and not necessarily to

annual average temperatures at a site. The four maize

cultivars of this study and most of the additional examples

were grown in common conditions with paired comparison

plants, so the observed efficiency differences are genetically

defined responses to environmental temperature, not a

consequence of differences in acclimation during growth.

Evidence That the “Futile” AOX

Reaction Supplies a TemperatureDependent Change in Substrate

Carbon Conversion Efficiency _____

Gonzalez-Meler and others (1999) measured the activities of AOX and COX in mung bean and soybean at two

temperatures. They showed (a) simultaneous and continuous engagement of AOX and COX pathways in both mung

bean and soybean (see also Hoefnagel and others 1995;

Guy and others 1989; Ribas-Carbo and others 1995), (b) relatively high activities of both AOX and COX at 14 °C and

28 °C, and (c) large differences in the temperature dependencies of AOX and COX and therefore different substrate

carbon conversion efficiencies at the two temperatures.

Thus, the thermodynamic requirement for a changing

efficiency with changing reaction temperatures can be

satisfied in part by the presence of the parallel AOX and

COX pathways. The remaining questions are: can the futile

reaction catalyzed by AOX (a) provide both a mechanism for

the thermodynamically required and experimentally observed changes in efficiency as temperature changes, and

(b) provide a means for quantitatively matching the efficiency change to requirements of a specific environment.

The studies of Gonzalez-Meler and others (1999) partially

answer these questions. With AOX and COX activity data

at only two temperatures, it is not possible to calculate

meaningful temperature coefficients, particularly when the

high temperature (28 °C) may be above the optimum temperature for growth of one or both species. However, the

limited available data do show large, species-dependent

differences in ratios of activities at the two temperatures.

To consider changes in substrate carbon conversion efficiencies specifically due to the effects of temperature on

activities of AOX and COX, we assume that plants with no

AOX activity operate with a substrate carbon conversion

efficiency near 0.7 (Stucki 1989), and that short-term, bidirectional, day-to-day changes in temperature affect the

AOX/COX ratio predominantly by differences in responses

to temperature rather than by other mechanisms (however,

see discussion below). Increasing the temperature from 14 to

28 °C increased the AOX/COX ratio for soybean but decreased the ratio for mung bean. Table 2 shows that soybean

ε increases from about 0.57 to 0.61 as temperature is increased between these two values, while ε for mung bean

decreases from 0.64 at 14 °C to 0.61 at 28 °C. Thus,

substrate carbon conversion efficiency changes with temperature in opposite directions for mung bean and soybean. ATP production efficiency of soybean increased at

Table 2—Calculated substrate carbon conversion efficiencies (ε) and growth rates for soybean and mung bean.

Soybean Mung bean

Growth rate as Growth rate as

T °C εa ε/(1-ε) RO2b (RO2 X ε/(1-ε)) ε ε/(1-ε) RO2 (RO2 X ε/(1-ε))

1X AOX

14 0.57 1.35 6.2 8.4 0.64 1.74 10.6 18.5

28 0.61 1.56 25.5 39.8 0.61 1.56 32.9 51.3

2X AOXc

14 0.45 0.82 9.4 7.7 0.60 1.51 13.4 19.9

28 0.50 1.00 42.5 42.5 0.56 1.30 44.5 57.7

aValues of ε were calculated from AOX and COX activities at 14 °C and 28 °C reported by Gonzalez-Meler and others (1999). The

calculations assume (a) a maximum substrate carbon conversion efficiency of 0.7 for both species when total respiration is via COX,

(b) production of 3 ATP per O2 via the COX pathway and 1 ATP per O2 via the AOX pathway, and (c) that substrate carbon conversion

efficiency is proportional to the total amount of ATP produced per mole O2 for plants containing both AOX and COX. b

RO2 is total oxidation rate via AOX plus COX. c

Values of ε in the presence of 2 x AOX are based on the reported near doubling of AOX activity with little change in COX activity

following cold acclimation of mung bean and soybean (Gonzalez-Meler and others 1999).
USDA Forest Service Proceedings RMRS-P-21. 2001 263

Responses of Plant Growth and Metabolism to Environmental Variables Predicted From Laboratory Measurements Hansen, Smith, Criddle, and Church

the higher temperature while efficiency was higher for

mung bean at the lower temperature. The similarities of

results in tables 1 and 2 show that a significant change in

efficiency with temperature for both warm and cold climate

plants could be accounted for by the presence of AOX and the

ratios of the temperature dependencies of AOX and COX.

Engagement of AOX Benefits Plants

Growing in Stress Conditions _____

An important consequence of temperature adaptation of

energy metabolism based on futile cycle mechanisms becomes apparent when the effect of AOX activity on growth

rate is considered. Growth rate is determined by the product

of the respiration rate (RCO2, or RO2 assuming the respiratory quotient = 1) multiplied by [ε/(1-ε)] (19). In the studies

of Gonzalez-Meler and others (1999) cold acclimation of

mung bean and soybean seedlings increased total oxidase

rate of both plants by increasing AOX about two-fold with

little change in COX activity. When AOX increases, the

overall oxidase rate is higher, substrate carbon conversion

efficiency is lower, but RCO2 multiplied by ε/(1-ε) is little

changed. Doubling AOX activity at 28 °C, soybean changes

growth rate only from 39.8 to 42.5 Cmol-1 s-1 mg-1 and mung

bean from 51.3 to 57.7 Cmol-1 s-1 mg-1 (table 2). Thus, growth

rate at a given temperature is little affected by increasing

(or decreasing) AOX because the changes in total respiration

rate are closely offset by reciprocal changes in the efficiency

of production of ATP per mole of O2 respired. Irrespective of

whether ε increases or decreases with temperature, growth

rate is essentially self-regulating. AOX synthesis or activation thus provides a mechanism for increasing electron flow,

without major effects on growth rate.

Mediation of the thermodynamically required changes in

substrate carbon conversion efficiency with changing temperature via introduction of futile reactions such as AOX can

have important benefits to cell survival. Engagement of

AOX can help maintain rapid electron flow (though at lower

efficiency) and plant viability when the COX pathway is

blocked or stressed. The continued flow of electrons via AOX

under temperature or other stress conditions that may

otherwise shut down respiration is consistent with the

previously proposed role of AOX in contributing to the

protection of cells from harmful oxidative reactions and

buildup of fermentation products when plants are stressed

(Wagner and Krab 1995; Purvis and Shewfelt 1993).

Stresses, by definition, hinder plant growth. The common

denominator linking all stresses is an effect on metabolism

that decreases energy use efficiency with increasing stress.

Any changes that differentially affect the rates of reactions

involving ATP synthesis and use triggers changes in the

requirement for futile cycling to maintain d[ATP]/dt = 0 and

a near constant phosphorylation potential. Thus, AOX (or

another reaction with similar effects) is required to “waste”

increasing amounts of energy in the presence of increasing

stress. In support of this conclusion, alternative oxidase has

been shown to be induced by many stresses including low

temperature, drought, some herbicides, hydrogen peroxide

and some protein synthesis inhibitors. Increasing AOX in

response to stress has correctly been discussed in context of

the need to maintain electron flow as a defense mechanism,

but the required role in changing energy coupling efficiencies to control phosphorylation potential and maintain viable cells has not been described.

The importance of AOX in providing means for response

to stress is emphasized in studies by Parsons and others

(1999). They demonstrated that, compared to control cells,

tobacco cells lacking alternative oxidase were greatly restricted in their ability to adapt to phosphate-limited growth.

The growth limitation was ameliorated by addition of an

uncoupling agent that provided (in the context of this communication) the “futile,” non-phosphorylating pathway necessary for adjustment of energy coupling stoichiometries

and phosphorylation potentials when AOX was absent. We

predict that the tobacco cells lacking AOX will also fail to

tolerate changing temperature and many other stress conditions. We propose that these cells are similar to homeotherms

that have more limited need for futile reactions because of

smaller changes in growth conditions.

Summary ______________________

As immobile ectotherms, plants must adjust energy metabolism to nearly continuous variation in temperature.

Thermodynamic arguments as well as experimental measurements show that this is accomplished via changing

stoichiometries of energy-coupled reactions and changing

energy use efficiencies. Adaptation of a plant to a particular

environment includes selection for the temperature coefficients for ATP synthesis, for anabolic use of ATP, and for

reactions wasting ATP or the potential to synthesize ATP

that allow phosphorylation potentials to be maintained

nearly constant over the required temperature range.

We have demonstrated that AOX activity can fill the

essential role of altering both the rate and efficiency of

respiratory metabolism in plant cells in response to temperature change. This is the mechanism by which AOX

fulfills the additional roles (mostly protective) that have

been ascribed to AOX (McCaig and Hill 1977; Parsons and

others 1999). Thus, whatever other functions it accomplishes, a primary role of AOX is maintenance of the

phosphorylation potential in the appropriate range for cell

viability when temperature changes. Variable temperature

requires all ectotherms to have enzymes with functions

analogous to the plant alternative oxidase. Ectothermic

animals that lack an alternative oxidase may satisfy this

requirement by a combination of uncoupling factors and

phosphatases, or analogous enzymes.

Alternative oxidase activity is adjusted by several factors

in addition to temperature. Concentrations of α-ketoacid

metabolites, disulfide reduction, oxidation state of quinones,

allosteric regulation, gene expression and possibly other

factors all fine-tune AOX activity (Buchanan and others

2000). Activity responses to some of these effectors may be

slow while others act rapidly and may be difficult to distinguish from simple Arrhenius temperature effects on enzyme

activity. Each could be expressed differentially as temperatures change. Thus, the presence of various activating

mechanisms of AOX can cause activity changes with temperature to differ from those calculated simply on the basis

of temperature coefficients for this discussion. However, all

of these moderators of AOX activity must work against a
264 USDA Forest Service Proceedings RMRS-P-21. 2001

Hansen, Smith, Criddle, and Church Responses of Plant Growth and Metabolism to Environmental Variables Predicted From Laboratory Measurements

background of nearly continuous, bi-directional temperature

change with instantaneous effects on enzyme activity that

change relative rates of AOX and COX activities, irrespective

of enzyme level and activation state. No matter what the

ultimate cause, AOX has a temperature dependence of activity that differs from the temperature dependence of COX and

the pattern of response to temperature differs with species,

cultivar, and genotype.

Unique consequences of altering respiration by variation in rates of AOX (or analogous “futile” reactions) are:

(a) Changing the level of AOX activity alters electron flow,

but the resulting changes in rates of electron flow and

changes in efficiency are offsetting so that there is a self

regulation of ATP availability for anabolism. Therefore,

growth rates at a given temperature are little changed by

alteration of AOX levels. (b) Via changes in AOX activity,

plant respiration rate may be increased to counter stress

effects, with an energy cost, but without altered growth rates

or major regulatory changes in other aspects of plant metabolism. (c) Because adjustment of efficiency with temperature

follows from the physical consequences of differences in

temperature coefficients of AOX and COX, no complex biological regulatory system need be involved to meet the

requirements of variable temperature. (d) Evolutionary adaptation of a plant to an environment by natural selection

must include selection for the relative values of temperature

coefficients of AOX and COX (in other words, efficiency

change with temperature) that optimize growth within that

environment.

Within photosynthesizing plant cells, chloroplasts also

have an ATP cycle with different temperature coefficients

for synthesis and use of ATP and must also maintain near

constant phosphorylation potentials for proper function.

Because there is no direct chemiosmotic link between chloroplasts and mitochondria, the chloroplasts require a separate class of futile cycle enzymes to maintain potentials

when reaction conditions change. Differences in temperature coefficients between Calvin cycle and photorespiration

activities (Mohr and Schopfer 1995) suggest that the “waste”

of ATP by photorespiration may be an important key to

maintaining phosphorylation potentials in chloroplasts

during variation in temperature. The necessary waste of

ATP in both mitochondria and chloroplasts suggests that

the many unsuccessful attempts to improve crop productivity by reduction of “wasteful” reactions such as AOX and

photorespiration can only achieve success for crops grown in

a narrow temperature range.

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USDA Forest Service Proceedings RMRS-P-21. 2001 265

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Lyneen C. Harris is an Undergraduate Student; M. Ajmal Khan is a

Visiting Professor; Jiping Zou is a Research Associate; Bruce N. Smith is a

Professor, Department of Botany and Range Science; Lee D. Hansen is a

Professor, Department of Chemistry and Biochemistry, Brigham Young

University, Provo, UT 84602.

Abstract—Plants that live in the desert playas of the Great Basin

must simultaneously tolerate very high concentrations of salt and

high temperature. This study characterizes the respiratory metabolism of one species growing in this environment. An isothermal calorimetric method was used to measure the dark metabolic

heat rate (q) and CO2 production rate (RCO2) of stem tissue from

Salicornia utahensis grown in the greenhouse or in constant

temperature growth chambers at six different concentrations of

NaCl solutions ranging from 0 to 1.0 M. Metabolic rates were

measured at eight temperatures from 5 to 40 °C. Temperature and

salt dependencies of q and RCO2 were used to model response of

both growth and substrate carbon conversion efficiency. Salt and

temperature stresses are not additive, but rather oppose one

another, in other words, the higher the salt, the higher the

temperature the plants will tolerate and vice versa. The maximum

temperature tolerated is an approximately linear function of salt

concentration, being about 20 °C at 0 M salt and about 32 °C at

1 M. Concentration of the endogenous osmoticant glycinebetaine

increased with salt and temperature but only to about 20 °C and

900 mM NaCl.

There are many indicators of stress responses of plants

such as chlorophyll fluorescence, heat shock proteins, and

osmoticant molecules. Each of these tells something about

the way a plant responds to a stress. Ultimately in order to

understand plant survival and growth, we must know how

the particular stress affects the energy metabolism (Smith

and others 2000). This study measured the effects of salt

(NaCl) and temperature on the biomass accumulation and

respiratory metabolism of a desert halophyte, Salicornia

utahensis Tidestr. This species is adapted to growth and

survival in wet, salty soils and a cold desert climate.

Growth of halophytes is stimulated by some level of

salinity (Flowers and others 1986), however growth of most

species is inhibited by too high salt concentrations, in other

words, greater than about 0.5 M NaCl, the concentration of

Effects of Salinity and Temperature on

Respiratory Metabolism of Salicornia

utahensis From a Great Basin Playa

Lyneen C. Harris

M. Ajmal Khan

Jiping Zou

Bruce N. Smith

Lee D. Hansen

salt in seawater (Ungar 1991). Previous studies on growth of

desert species (Atriplex griffithii, Halopyrum mucronatum,

Haloxylon recurvum, and Sueda fruticosa) from Pakistan

showed that low salinities promoted growth (Khan and

others 1998). Increasing salt to 425 mM promoted growth of

Cressa cretica but growth in 850 mM salt was not significantly different from controls grown without added salt

(Khan and Aziz 1998). Growth of halophytes from the Great

Basin in Western North America (Salicornia rubra, Salicornia utahensis, Suaeda torreyana, Allenrolfea occidentalis)

shows a similar pattern of promotion at moderate salinities

(400 to 600 mM NaCl) and a decline with further increases

in salinity (Khan and others 2000).

Halophytes usually absorb a considerable amount of salt

to maintain osmotic balance with their highly saline medium. The most salt tolerant species have high internal salt

concentrations, suggesting that the ability of the cells to

tolerate high salt concentrations is at least as important

to survival as the ability to restrict accumulation of salt

(Flowers and others 1977). However, the enzymes of halophytes, unlike those of salt tolerant bacteria, are inhibited

by high salt concentrations suggesting that cytoplasmic

enzymes are protected from salt either by sequestration of

salt in cell walls and vacuoles (Weber and others 1977) or by

protective solutes such as glycinebetaine, proline, polyols, or

cyclitols (Flowers and others 1977).

Seed germination of Triglochin maritima from the Great

Basin was most inhibited by exposure to high salinities at

suboptimal thermoperiods (Khan and Ungar 1999). For

halophytes Salicornia rubra, S. utahensis, Distichlis

spicata, and Allenrolfea occidentalis growing in the field

showed the highest metabolism, respiration, efficiency, and

growth during May and June and lowest during the hot, dry

month of August (Harris and others, in press). By contrast,

Salicornia europaea from a salt marsh in Ohio germinated

better following rain events in June than earlier in the year

(Egan and Ungar 1999).

Except for the fact that S. utahensis is a common plant in

the Great Basin desert with cold winters, hot summers, and

large diurnal temperature changes (commonly 20 to 30 °C),

little is known about the temperature tolerance of this

species. During the period of high summer temperatures,

which is also the time of least rainfall, water evaporates

from the shallow playas, increasing salt concentration in

the soil. It was thus of interest to examine the combined

effects of temperature and salt. In their saline environment,
266 USDA Forest Service Proceedings RMRS-P-21. 2001

Harris, Khan, Zou, Smith, and Hansen Effects of Salinity and Temperature on Respiratory Metabolism of Salicornia utahensis From a Great Basin Playa

halophytes are normally exposed to multiple stresses. In

addition to salt and temperature stresses, there is often a

low osmotic potential of water and a low partial pressure of

oxygen due to standing water or a high water table (Ungar

1991). Presumably the imposition of one kind of stress

reduces tolerance to other simultaneous stresses, a hypothesis looked at in this study. This study examines the interaction of both low and high salt and temperature stresses.

Predicted biomass accumulation and characteristics of energy metabolism are used as indicators of stress response.

Aerobic respiration has two aspects: catabolism and anabolism. In catabolism, organic substrates are oxidized to produce CO2. Part of the energy produced by oxidation is used

to convert ADP and inorganic phosphate to ATP, the rest is

lost as heat.

substrate + O2 + ADP + Pi → CO2 + H2O + ATP + heat (1)

ATP produced in catabolism is transient, but is used for

cellular work, including anabolism as shown below:

substrate + ATP → growth + ADP + Pi

 + heat (2)

In anabolism, heat and new plant tissue are produced and

ATP is hydrolyzed back to ADP and phosphate. A calorimeter measures the rate of heat loss (q) from both catabolism

and anabolism. The rate of CO2 production (RCO2) measures

the rate of catabolism. With carbohydrate as the specific

substrate, predicted growth rate of structural biomass or

rate of anabolism (RSG) is thus related to the difference in

two measured variables as in equation 3,

RSG∆HB = 455RCO2 – q (3)

where ∆HB is the enthalpy change for the formation of

biomass from photosynthate and Thornton’s constant (–455 ±

15 kJ mol–1 of O2) is incorporated to calculate the rate of

energy generated by catabolism. Thus, growth rate in terms

of energy is proportional to the difference between the

measured values of RCO2 and q. The temperature dependencies of RCO2 and q are different (Hansen and others 1994).

The difference between 455RCO2 and q therefore changes

with temperature and this difference can be used to predict

growth rate changes with temperature (Criddle and others

1997).

Predicted specific growth rate may also be expressed as a

function of the substrate carbon conversion efficiency (ε) and

respiration rate (RCO2).

RSG = RCO2[ε/(1–ε)] (4)

Combining equations 3 and 4 to eliminate RSG gives equation 5,

[ε/(1–ε)]∆HB = –q/RCO2 – (1–γP/4)455 (5)

which relates the ratio of q/RCO2 to ε. Values of q/RCO2

measured as a function of temperature can thus provide

information on substrate carbon conversion efficiency (ε)

and the oxidation state of the substrate carbon, in other

words, γP (Hansen and others 1994).

The purpose of this work is to examine how an extreme

halophyte adapts its respiratory metabolism to temperature

and salinity conditions common in its native habitat. In this

study, calorimetry was used to determine the high and low

stress temperatures and salinities for Salicornia utahensis

grown in controlled conditions. When the metabolic heat

rate exceeds energy made available through catabolism of

carbohydrate, the plant is considered to be stressed (Smith

and others 2000).

Materials and Methods ___________

Seeds of Salicornia utahensis Tidestr. were collected during the fall of 1995 from salt playas 1–2 km east of Goshen,

Utah. Seeds were separated from the inflorescence, surface

sterilized using the fungicide Captan, and stored at 4 °C.

Seeds were germinated in 36 cm2 pots filled with sand and

placed in trays of distilled water to sprout. Once sprouted,

salt was introduced into the trays and increased by 200 mM

every 2 days until desired salinity was reached. Ten pots

each were grown at 0, 200, 400, 600, 800, and 1,000 mM

NaCl. A half-strength Hoagland solution was used to supply

nutrients. Pots were subirrigated and the water level adjusted daily to correct for evaporation. Salt solutions were

completely replaced once a week to avoid buildup of salinity

in the pots. Plants were grown in a greenhouse at a daytime

mean temperature of 25 °C and a mean nighttime temperature of 15 °C. Metabolic heat rates (q) and respiration rates

(RCO2) and fresh and dry weights of plant shoots were

measured 60 days after the highest salt concentration was

reached.

Another set of plants was sprouted as above but grown at

six different salinities in each of four controlled environmental chambers maintained at 10, 20, and 30 °C with a 12-hour

photoperiod (200 μmol m–2 s–1, 400–700 nm). Plants were

harvested after about 5 months.

Plants were cut just below the cotyledon and about 100 mg

fresh wt. of tissue was placed in each of three ampules of a

microcalorimeter (Hart Scientific model 7707 or Calorimetry Sciences Corporation model 4100). After 15 to 20 minutes thermal equilibration at the desired temperature, the

metabolic heat rate (q) was measured for another 15 to 20

minutes. The ampules were removed from the calorimeter

and a small vial filled with 40 μl of 0.4 M NaOH placed in the

calorimeter ampule with the tissue. Again a 15–20 minute

thermal equilibration was necessary, followed by measurement of the sum of the heat rate from metabolism and CO2

reaction with the NaOH (–108.5 kJ mole–1) for 15–20 minutes. After the NaOH was removed, the heat rate (q) is

measured again as before (Hansen and others 1994; Criddle

and others 1997). The difference in the measurements with

and without NaOH solution gives the rate of CO2 evolution

(RCO2) by the plant tissue. The tissue was then run at

another temperature. Measurements were made on each

sample at 9 temperatures: 5, 10, 15, 20, 25, 30, 35, 40, and

45 °C.

For glycinebetaine measurements, the method of Gorham

(1984) was followed. Plant material (0.5 g) was boiled in

10 ml of water for 2 hours at 100 °C in a dry heat bath.

Samples were diluted with a 50 mM potassium dihydrogen

phosphate buffer adjusted to pH 4.6. This was the carrier

buffer that was also used in the HPLC system. The sample

was cooled and filtered using a 0.45 μm membrane filter

(Gelman, Ann Arbor, MI), and then used directly to measure

glycinebetaine with a Hewlett Packard 1050 modular 3D

HPLC (Boise, ID) with quaternary pump, online degasser,

autosampler, and a diode array detector with a stainless

steel flow cell (6-mm path length, 8 μl volume). Separations

were performed on a 250 x 4 mm i.d. stainless steel column
USDA Forest Service Proceedings RMRS-P-21. 2001 267

Effects of Salinity and Temperature on Respiratory Metabolism of Salicornia utahensis From a Great Basin Playa Harris, Khan, Zou, Smith, and Hansen

Table 1—Endogenous levels of glycinebetaine in seedlings of

Salicornia utahensis grown in different NaCl concentrations

in the greenhouse.

NaCl concentrations, mM g glycinebetaine/kg dry wt.

0 28.5

300 48.8

600 45.6

900 44.4

1,200 37.0

1,500 47.6

Table 2—Endogenous levels of glycinebetaine in seedlings of

Salicornia utahensis grown at different temperatures in

growth chambers in different NaCl concentrations.

Growth Salinity Glycinebetaine

temperature mM NaCl g/kg dry weight

10 °C 0 34.4

300 32.3

900 46.3

1,500 35.7

20 °C 0 14.9

300 57.1

900 59.4

1,500 37.7

30 °C 0 ND

300 54.2

900 died

1,500 died

packed with 10 μm Nucleoside 100-10SA (Phenomenex,

Torrance, CA). Flow rate was 1.2 ml min–1. Glycinebetaine

standards were run at 1, 10, and 100 mmol l–1.

Results and Discussion __________

Glycinebetaine concentrations (table 1) increased from

28.5 g glycinebetaine per kg dry wt. of plant tissue for

Salicornia utahensis grown in zero salt to 48.8 g/kg for

plants grown in the greenhouse in 300 mM NaCl. Increases

in salinity above 300 mM had essentially no effect on the

glycinebetaine concentration within the plant tissue. Temperatures at which the plants were grown (table 2) did affect

glycinebetaine concentration. Compared with plants grown

in zero salt at 20 °C, plants grown without salt at 10 °C had

more than twice the concentration of glycinebetaine. Perhaps the glycinebetaine was not functioning as an osmoticant in this case. Unlike some reports in the literature (Khan

and others 1998), there was not a linear increase in

glycinebetaine with salt exposure. Other osmoticants exist

(Flowers and others 1977) and may be operative as well here.

Weber and others (1977) did show that salt tolerance in

Salicornia utahensis was based on exclusion of salt from the

photosynthetic cells and on the ability of the succulent stem

to function even though sections were dead owing to high

salt concentration. It may be that glycinebetaine operates at

relatively low concentrations of NaCl but that active accumulation of salt into certain tissues occurs with higher

concentrations of external salt and possibly at higher

temperatures.

Figure 1 is a plot of the metabolic heat rate as a function of

salt concentration at the various temperatures. The data

show the heat rate generally increases with increasing

Figure 1—Plot of dark metabolic heat rate q versus the NaCl concentration in which the plants

were grown. Each line presents the measurements made at the indicated temperature.
268 USDA Forest Service Proceedings RMRS-P-21. 2001

Harris, Khan, Zou, Smith, and Hansen Effects of Salinity and Temperature on Respiratory Metabolism of Salicornia utahensis From a Great Basin Playa

temperature up to 35 to 40 °C after which it decreases

markedly. Metabolic heat rate generally decreases with increasing salt, the effect becoming more pronounced with

increasing temperature.

Figure 2 is a plot of the respiratory CO2 rate (RCO2) as a

function of salt concentration at the various temperatures.

RCO2 increases with temperature at low temperatures, goes

through a maximum at intermediate temperatures, then

decreases at higher temperatures. Salt has little effect on

RCO2 except at very low (≤5 °C) and very high (>35 °C)

temperatures where RCO2 increases sharply.

Predicted growth of S. utahensis seedlings generally increased with salt concentrations (fig. 3), with high temperatures showing the largest effect of increasing salt.

Figure 2—Plot of dark metabolic CO2 rate versus the NaCl concentration in which the

plants were grown. Each line presents the measurements made at the indicated

temperature.

Figure 3—Specific growth rate, ∆HBRSG, calculated from metabolic heat and CO2 rates

as a function of the salt concentration in the growth medium.
USDA Forest Service Proceedings RMRS-P-21. 2001 269

Effects of Salinity and Temperature on Respiratory Metabolism of Salicornia utahensis From a Great Basin Playa Harris, Khan, Zou, Smith, and Hansen

Plotting the same data another way (fig. 4), averaging the

growth for all salt concentrations at each temperature predicts a decrease in growth with increasing temperature. The

two data points at 1,000 mM NaCl at 40 and 45 °C are

anomalous in both figures 3 and 4. These two points at high

values of ∆HBRSG do not indicate high growth rates, instead

these values are a result of the imposed stress and indicate

the production of catabolic products other than CO2.

Figure 5 is a contour plot of the specific growth rate,

∆HBRSG, calculated from metabolic heat and CO2 rates as a

function of the measurement temperature and salt concentration in the growth medium. The synergism between these

Figure 5—Contour plot of the specific growth rate, ∆HBRSG, calculated

from metabolic heat and CO2 rates as a function of the measurement

temperature and salt concentration in the growth medium.

Figure 4—Specific growth rate, ∆HBRSG, calculated from metabolic heat

and CO2 rates as a function of the measurement temperature.
270 USDA Forest Service Proceedings RMRS-P-21. 2001

Harris, Khan, Zou, Smith, and Hansen Effects of Salinity and Temperature on Respiratory Metabolism of Salicornia utahensis From a Great Basin Playa

two environmental variables can be deduced from this plot.

Contrary to our intuitive assumption that high temperature

and high salt would be more stressful than either stress

alone, the results show that the two together are less

stressful than either high salt or high temperature alone.

This is shown by the approximately linear diagonal of

maximum tolerable temperatures that runs from about 20

°C at 0 salt to about 30 °C at 1,000 mM salt on the contour

plot. Note that RSG∆HB tends toward negative values to the

right of this diagonal.

The major conclusion of this paper agrees with the natural

history of S. utahensis. In the Great Basin, precipitation

occurs primarily during early spring (April-May) and late

fall (October-November) when temperatures are typically

around 5 °C at night and 20 to 25 °C during the day. Thus,

the salt in the playas is most dilute during periods with these

temperatures. In the summer, when daytime air temperatures range up to about 45 °C, is also when the salt is most

concentrated. The data collected in this study show that

Salicornia utahensis respiratory metabolism is well adapted

to these conditions, that is, to lower salt concentrations at

low temperatures and higher salt concentrations at higher

temperatures. The details of how the species has accomplished the feat of adapting to the sum of two apparently

deleterious stresses are certainly not clear as yet.

Halophytes are normally “includers” (in other words, they

are generally in equilibrium with the salt in solution in the

root environment), and thus there is probably little or no

extra energy cost for operating in a variable, high-salt

environment. Tertiary structures of proteins and membranes must however be appropriate for the environment.

In summary, the methods employed in this study have

contributed to the understanding of the phenomenon of salt

stress by providing information on the synergism between

salt and temperature.

References _____________________

Criddle, R. S.; Smith, B. N.; Hansen, L. D. 1997. A respiration

based description of plant growth rate responses to temperature. Planta. 201: 441–445.

Egan, T. P.; Ungar, I. A. 1999. The effects of temperature and

seasonal change on the germination of two salt marsh species,

Atriplex prostrata and Salicornia europaea, along a salinity

gradient. International Journal of Plant Science. 160: 861–867.

Flowers, T. J.; Troke, P. F.; Yeo, A. R. 1977. The mechanism of salt

tolerance in halophytes. Annual Review of Plant Physiology. 28:

89–121.

Gorham, J. 1984. Separation of plant betaines and their sulphur

analogues by cation-exchange high-performance liquid chromatography. Journal of Chromatography. 287: 345–351.

Hansen, L. D.; Hopkin, M. S.; Rank, E. R.; Anekonda, T. S.;

Breidenbach, R. W.; Criddle, R. S. 1994. The relation between

plant growth and respiration: a thermodynamic model. Planta.

194: 77–85.

Harris, L. C.; Gul, B.; Khan, M. A.; Hansen, L. D.; Smith, B. N.

[In press]. Seasonal changes in respiration of halophytes in

salt playas in the Great Basin, U.S.A. Wetlands Ecology and

Management.

Khan, M. A.; Aziz, S. 1998. Some aspects of salinity, density, and

nutrient effects of Cressa cretica. Journal of Plant Nutrition. 21:

769–784.

Khan, M. A.; Gul, B.; Weber, D. J. 2000. Germination responses of

Salicornia rubra to temperature and salinity. Journal of Arid

Environments. 45: 207–214.

Khan, M. A.; Ungar, I. A. 1999. Effect of salinity on seed germination

of Triglochin maritima under various temperature regimes.

Great Basin Naturalist. 59: 144–150.

Khan, M. A.; Ungar, I. A.; Showalter, A. M.; Dewalt, H. D. 1998.

NaCl-induced accumulation of glycinebetaine in four subtropical

halophytes from Pakistan. Physiologia Plantarum. 102: 487–492.

Smith, B. N.; Criddle, R. S.; Hansen, L. D. 2000. Plant growth,

respiration and environmental stress. Journal of Plant Biology.

27: 89–97.

Ungar, I. A. 1991. Ecophysiology of vascular halophytes. Boca

Raton, FL: CRC Press. 209 p.

Weber, D. J.; Rasmussen, H. P.; Hess, W. M. 1977. Electron microprobe

analyses of salt distribution in the halophyte Salicornia pacifica var.

utahensis. Canadian Journal of Botany. 55: 1516–1523.
USDA Forest Service Proceedings RMRS-P-21. 2001 271

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

V. Wallace McCarlie is a Research Assistant for Lee D. Hansen and

Bruce N. Smith, Department of Chemistry and Biochemistry; Lee D.

Hansen is a Professor, Department of Chemistry and Biochemistry; Bruce

N. Smith is a Professor, Department of Botany and Range Science,

Brigham Young University, Provo, UT 84602.

Abstract—Cheatgrass (Bromus tectorum L.) is a dominant weed

that has increased the frequency of wildfire in the Great Basin since

its introduction approximately 106 years ago. Characteristics of

respiratory metabolism were examined in eleven subpopulations

from different habitats. Seeds from each subpopulation were germinated (4mm radicle) and metabolic heat rates (q) and respiration

rates (RCO2) determined calorimetrically at 5 °C intervals from 5 to

30 °C or from 5 to 45 °C. From the experimental data, growth rates

and ratios of q/RCO2 (a measure of efficiency) were calculated. In

general, growth rate increases from a low temperature limit of 3 to

7 °C to an upper temperature limit between 27 to 31 °C. Beyond

these limits growth ceases. These limits differ among subpopulations, and are related to the native microclimate.

Introduction ____________________

Since its Eurasian origins—introduced from the eastern

Mediterranean area of Europe into the United States—

cheatgrass (Bromus tectorum L.) has become one of the most

troublesome weeds in the western United States (Upadhyaya

and others 1986). Furthermore, cheatgrass—more than any

other plant—has transformed the vegetative landscape in

the Great Basin and Columbia Basin areas since its introduction approximately 106 years ago (Upadhyaya and others 1986; Klemmedson and Smith 1964). Despite a few

advantageous characteristics, such as being high-quality

forage in the early spring for grazing animals, and the fact

that its dense root growth and expansive top growth prevent

erosion, the disadvantages of cheatgrass—in relation to the

environment and other native perennial plants—far outweigh the advantages (Morrow and Stahlman 1984).

Cheatgrass appears to have an extraordinary ability to

adapt to a variety of microclimates. Some studies suggest

that cheatgrass grows well, even under low-nitrogen situations (Klemmedson and Smith 1964). Additional studies

suggest that, though water is a limiting factor in the

growth of cheatgrass, its ability to thrive under relatively

Respiratory and Physiological

Characteristics in Subpopulations

of Great Basin Cheatgrass

V. Wallace McCarlie

Lee D. Hansen

Bruce N. Smith

low-water conditions is superior to perennial grasses. If

moisture levels allow seed production, the germination rate

of stressed seed is unchanged relative to seed produced

under normal conditions (Richardson and others 1989).

As early as 1955, striking phenotypic variation was observed in cheatgrass (Klemmedson and Smith 1964). Moreover, a few studies conducted during the 1990s provide

evidence for not only phenotypic variation (Meyer and Allen

1999), but also genetic variation within populations (Hemming and others 1999), and more robustly between populations (Novak and others 1991, 1993; Novak and Mack 1993;

Mack and Pyke 1983, 1984). According to Novak and Mack

(1993) genetic differentiation is greater between populations because cheatgrass has very high levels of inbreeding,

which reduces the chance for recombination of the genome.

Nevertheless, cheatgrass appears to be capable of adapting

to a variety of climates and can do so even with low levels of

water, relative to other native species.

Throughout the western United States, cheatgrass has

invaded crop plants such as winter wheat (Triticum aestivumL.) and alfalfa (Medicago sativaL.) ( Morrow and Stahlman

1984). A number of factors have contributed to this invasion—both in crop plants and undeveloped habitats. Wild

fires and soil-nutrient depletion have been suggested, yet

overall it becomes apparent that no matter how cheatgrass

initially gained a foothold in the western United States, its

ability to adapt and take over native habitats has increased.

As Nasri and Doescher (1995) point out in their study of

Idaho fescue, increased competition from cheatgrass depleted soil moisture available for the fescue and consequently reduced Idaho fescue’s growth substantially. Further validating this claim, Evans and Young (1984) argue

that cheatgrass was one of three alien grasses that established, dominated, and revolutionized plant succession in

the sagebrush grasslands in the western United States.

Even during the 1960s Klemmedson and Smith (1964)

observed that cheatgrass’ physiological responses were much

quicker than their native perennial grass counterparts.

Fire, growth periods, and its physiological characteristics

give cheatgrass a competitive advantage. The caryopes of

cheatgrass are essentially fireproof and as it ends its

growth cycle the extremely high flammability of the grass

permits fires to start and spread with unusual rapidity.

Cheatgrass seeds are protected while other perennial grass

seeds are made impotent. Cheatgrass has added to the fire

cycle: over a century ago, fire-return intervals on the sagebrush-steppe in Idaho’s Snake River Plains fluctuated anywhere from 35 to 100 years. Now, because cheatgrass creates

a more continuous fuelbed, the fire-return interval is very
272 USDA Forest Service Proceedings RMRS-P-21. 2001

McCarlie, Hansen, and Smith Respiratory and Physiological Characteristics in Subpopulations of Great Basin Cheatgrass

short—anywhere from 2 to 4 years (Whisenant 1990). Furthermore, native plants, such as sagebrush do not have a

quick capability to regenerate after a fire has devoured

native habitats. Fire enhances the establishment of

cheatgrass: while everything else is trying to regenerate—

slowly—cheatgrass is back the next spring taking over the

decimated lands. Since its growth season includes germination in the fall after autumn rains (Beckstead and others

1995), overwintering in the vegetative stage, and completing growth in the early spring, cheatgrass gets first track on

available water and nutrients in the soil. Additionally,

following rapid germination in the fall, cheatgrass quickly

establishes an extensive fibrous root system that continues

to grow through the winter (Thill and others 1984). Finally,

even under drought conditions cheatgrass will mature sufficient seed to ensure plants for the following year

(Klemmedson and Smith 1964).

From its Eurasian origins cheatgrass has adapted to the

Great Basin remarkably quickly. If the restoration of native

ecosystems is a primary goal, cheatgrass is one of the

primary culprits in impoverishing native ecosystems of their

natural species (Billings 1990; D’Antonio and Vitousek 1992);

therefore, the physiology of cheatgrass must be understood.

This study reflects an effort to understand the respiratory

physiology of cheatgrass and its adaptation to the Great

Basin.

In this study, the respiratory characteristics of cheatgrass

subpopulations are determined by calorimetric techniques

and analyzed with a model of plant growth first introduced

nearly a decade ago (Criddle and others 1991, 1994, 1996,

1997; Criddle and Hansen 1999; Hansen and others 1994,

1997, 1998a, 1998b; Smith and others 1999, 2000). Since

growth rates are functions of energy metabolism, calorimetry is necessary to understand plant metabolic physiology

(Hansen and others 1994). Plant metabolic calorimetry

might be defined as the thermodynamic study of physiological processes.

Materials and Methods ___________

Caryopes from eleven subpopulations of cheatgrass in the

Great Basin were used in this study. Nine of the eleven

subpopulations came from Utah; the other two originate in

Colorado and Nevada (table 1). The United States Department of Agriculture, Forest Service Shrub Sciences Laboratory, at Provo, Utah, provided the caryopes for this analysis.

The caryopes were greenhouse-grown progeny of a number

of maternal lines. The original seeds were collected in 1995

and this study conducted on seeds produced in 1998 and

1999. Seeds from each subpopulation were placed on petri

dishes, dampened with distilled water, and germinated at

20 °C. Germinated seedlings’ respiratory characteristics

were measured when 2 to 5 days old.

Data were collected with calorimeters: Calorimetry Sciences Corporation model 4100 and Hart Scientific model

7707. RCO2 and q were determined at temperatures from 5 to

45 °C. These determinations came from (a) placing 80 to 150

mg (15 to 30 seeds) of germinated caryopes into 1-ml calorimeter ampules; (b) setting a desired temperature and waiting

approximately 20 minutes for a steady-state heat rate; (c)

placing a 40 μl vial of 0.4M NaOH in the ampule and again

waiting for a steady-state heat rate, which now includes both

metabolic heat and heat from the reaction of carbon dioxide

and sodium hydroxide to produce carbonate; (d) removing

the vial of NaOH and again waiting for a steady-state; and

(e) repeating the process at another temperature. Measurements were done in the order of 20, 15, 10, and 5 °C on one

sample and at 25, 30, 35, 40, and 45°C on another. Data were

analyzed by averaging the heat rates directly measured in

steps b and d, to obtain the metabolic heat rate q, subtracting this from the heat rate measured in step c, and

dividing this difference by the enthalpy change for the reaction, –108.5 kJ mol–1, which gives RCO2. The ratio of q/ RCO2

was calculated from average values of q and RCO2 obtained

in approximately 5 replicates.

Thermodynamic Model

Growth rates were calculated from equation 1

RSG∆HB = 455RCO2 – q (1)

where RSG is the specific growth rate in moles of carbon per

gram of tissue per second, and ∆HB is the enthalpy change

for formation of structural biomass from substrate in kilojoules per mole of carbon. The constant, 455 kJ mol–1 CO2,

comes from Thornton’s rule by assuming carbohydrate is the

substrate. Note that under conditions where q is greater

than 455RCO2, RSG∆HB will be negative, indicating conditions of no growth.

Results ________________________

After replicating the experiment several times on each

subpopulation and thereby providing mean data from about

100 caryopes per temperature, the data were analyzed for

distinct differences in the physiological responses to temperature. Figures 1, 2 and 3 show plots of metabolism of

subpopulations that, in general, are indicative of the response of other subpopulations to temperature. Figure 4

shows q/RCO2 averaged over the subpopulations as a function of temperature. Figure 5 depicts the calculated growth

rate as a function of temperature averaged over the 11

subpopulations. Table 2 provides Arrhenius slopes for q and

RCO2 (Criddle and Hansen 1999).

Table 1—Eleven subpopulations of cheatgrass (Bromus tectorum L.)

in the Great Basin: classified by sites of origin.

Subpopulation County State Altitude

St. George Washington Utah 850 m

Green River Emery Utah 1,280 m

Whiterocks Tooele Utah 1,450 m

Ephraim Sanpete Utah 1,740 m

Hobble Creek Utah Utah 1,800 m

Potosi Clark Nevada 1,850 m

Castle Rock Douglas Colorado 1,980 m

Salina Sevier Utah 2,040 m

Strawberry Wasatch Utah 2,400 m

Fairview Sanpete Utah 2,770 m

Nebo Summit Utah Utah 2,850 m
USDA Forest Service Proceedings RMRS-P-21. 2001 273

Respiratory and Physiological Characteristics in Subpopulations of Great Basin Cheatgrass McCarlie, Hansen, and Smith

Figure 1—Metabolic heat rate (open circle) and

RCO2 production rate (closed circle) as function of

temperature for the St. George subpopulation.

Figure 2—Metabolic heat rate (open circle) and

RCO2 production rate (closed circle) as function of

temperature for the Nebo Summit subpopulation.

Figure 3— Metabolic heat rate (open circle) and

RCO2 production rate (closed circle) as function of

temperature for the Salina subpopulation.

Figure 4—Averaged q/RCO2 ratios for eleven subpopulations of cheatgrass as functions of temperature. This ratio demonstrates, in general, the efficiency

of cheatgrass throughout the Great Basin in converting substrate into biomass. Lower values translate

into greater efficiency.
274 USDA Forest Service Proceedings RMRS-P-21. 2001

McCarlie, Hansen, and Smith Respiratory and Physiological Characteristics in Subpopulations of Great Basin Cheatgrass

Discussion _____________________

In this study, it has become apparent that although the

subpopulations are different from one another in terms of

temperature response (table 2), there are also some general

conclusions. Cheatgrass barely grows at 5 °C (fig. 5), and is

very inefficient in doing so (fig. 4). Furthermore, the optimum growth temperature is between 10 and 20 °C. Moreover, cheatgrass’ growth rate is apparently a bi-phasic

Table 2—Arrhenius slopes μq and μCO2 that represent physiological responses to temperature, along with temperature range. Differences

between slopes are related to the different microclimates at the site of origin.

Subpopulations μq, kK–1 ∆T μCO2, kK–1 ∆T μq, kK–1 ∆T μCO2, kK–1 ∆T

St. George 7.5 5 to 20 °C 10.1 5 to 10 °C 5.0 25 to 30 °C 5.3 15 to 20 °C

Green River 6.4 5 to 30 °C 17.0 5 to 10 °C –0.8 35 to 40 °C 4.7 15 to 30 °C

Whiterocks 7.0 5 to 10 °C 13.1 5 to 15 °C 14.1 15 to 20 °C –1.2 20 to 25 °C

Ephraim 7.2 5 to 15 °C 3.1 5 to 15 °C 4.6 20 to 30 °C 4.4 20 to 30 °C

Hobble Creek 7.8 5 to 15 °C 7.4 5 to 20 °C 4.3 20 to 30 °C 0.7 25 to 30 °C

Potosi 7.8 5 to 15 °C 6.6 5 to 20 °C 4.3 20 to 30 °C 3.0 25 to 30 °C

Castle Rock 7.4 5 to 20 °C 22.4 5 to 10 °C 3.5 25 to 35 °C 3.6 15 to 35 °C

Salina 6.1 5 to 15 °C 8.9 5 to 20 °C 4.1 20 to 30 °C 2.1 25 to 30 °C

Strawberry 7.2 5 to 30 °C 2.0 5 to 10 °C –1.4 35 to 40 °C 6.4 15 to 30 °C

Fairview 5.4 5 to 30 °C 10.2 5 to 10 °C 0.3 35 to 40 °C 3.1 15 to 25 °C

Nebo Summit 5.3 5 to 15 °C 10.0 5 to 15 °C 4.5 20 to 30 °C 4.0 20 to 30 °C

Figure 5—Calculated growth rate as a function of

temperature averaged across eleven subpopulations.

Depicts, in general, both low and high extreme temperature limits to growth.

function, that is, at lower temperatures cheatgrass has a

different physiological response or combination of responses, than at higher temperatures (figs. 1-3; table 2).

Cheatgrass stops growing between 30 and 40 °C.

Another interesting finding is that, at very low temperatures (in other words around 5 °C) cheatgrass appears to

waste a lot of energy in burning lipid as an energy substrate

for growth as shown by the value of q/RCO2 greater than

455 at 5 °C (figure 4). Carbohydrate is a free fuel, in terms

of energy expended, to an autotrophe; whereas lipid costs a

substantial amount of energy to produce energy that could

theoretically be used to produce more biomass. The drop in

q/RCO2 from 5 to 10 °C indicates a switch to carbohydrate by

10 °C.

Cheatgrass has adapted (or adapts) to grow at temperatures extant when water is available. For example, St. George

(fig. 1) cheatgrass is adapted to grow at some of the lowest

temperatures relative to the other subpopulations. Thus,

instead of growing in April, May, and June, the St. George

growth temperatures loosely correlate with environmental

temperatures in February, March, and April when rainfall

occurs at this site, where by May available water is reduced

by 65 percent. This means then, in general, that subpopulations, which experience the hottest climates, are adapted

to the coldest temperatures. Therefore, we see that

cheatgrass’ respiratory metabolism is closely aligned with

its environment.

Now, though we have said that cheatgrass has adapted

to its specific environment, individuals cannot adapt to

transplanted environments—we must remember that

cheatgrass was only introduced approximately 106 years

ago, and in many areas less. Nevertheless, cheatgrass

grouped-progeny (stands) appear to have the capability to

adapt rapidly to microclimates. The response to climate is

clearly not a short-term acclimation or even acclimation of

first or second-generation progeny or the subpopulation

differences observed would not be present in the greenhouse-grown seed used in this study. A full analysis of

temperatures at each site during the growth season for

cheatgrass is expected to show that the Arrhenius slopes

for each population are correlated with site temperature

and temperature variability.
USDA Forest Service Proceedings RMRS-P-21. 2001 275

Respiratory and Physiological Characteristics in Subpopulations of Great Basin Cheatgrass McCarlie, Hansen, and Smith

References _____________________

Beckstead, J.; Meyer, S. E.; Allen, P. S. 1995. Effects of afterripening

on cheatgrass (Bromus tectorum) and squirreltail (Elymus

elymoides) germination. In: Roundy, B. A.; McArthur, E. D.;

Haley, J. S.; Mann, D. K., comps. Proceedings: wildlife shrub and

arid land restoration symposium. Gen. Tech. Rep. INT-GTR-315,

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Research Station: 165–172.

Billings, W. D. 1990. Bromus tectorum, a biotic cause of ecosystem

impoverishment in the Great Basin. In: Woodwell, G. M., ed. The

Earth in transition: patterns and processes of biotic impoverishment. Cambridge: Cambridge University Press: 301–322.

Criddle, R. S.; Smith, B. N.; Hansen, L. D. 1997. A respiration based

description of plant growth rate responses to temperature. Planta.

201: 441–445.

Criddle, R. S.; Hansen, L. D. 1999. Calorimetric methods for analysis of plant metabolism. In: Kemp, R. B., ed. Handbook of thermal

analysis and calorimetry, vol. 4: from macromolecules to man.

Amsterdam: Elsevier Science B. V.

Criddle, R. S.; Breidenbach, R. W.; Fontana, A. J.; Henry, J-M.;

Smith, B. N.; Hansen, L. D. 1996. Plant respiration responses to

climate determine geographic distribution. Russian Journal of

Plant Physiology. 43: 698–704.

Criddle, R. S.; Breidenbach, R. W.; Hansen, L. D. 1991. Plant

calorimetry: how to quantitatively compare apples and oranges.

Thermochimica Acta. 193: 67–90.

Criddle, R. S.; Hopkin, M. S.; McArthur, E. D.; Hansen, L. D. 1994.

Plant distribution and the temperature coefficient of metabolism.

Plant and Cell Environment. 17: 233–243.

D’Antonio, C. M.; Vitousek, P. M. 1992. Biological invasions by

exotic grasses, the grass/fire cycle, and global change. Annual

Review of Ecology and Systematics. 23: 63–87.

Evans, R. A.; Young J. A. 1984. Microsite requirements for downy

brome (Bromus tectorum) infestation and control on sagebrush

rangelands. Weed Science. 32(supplement 1): 13–17.

Hansen, L. D.; Smith, B. N.; Criddle, R. S. 1998a. Calorimetry of

plant metabolism: a means to rapidly increase agricultural biomass production. Pure and Applied Chemistry. 70: 687–694.

Hansen, L. D.; Smith, B. N., Criddle, R. S.; Breidenbach, R. W.

1998b. Calorimetry of plant respiration. Journal of Thermal

Analysis. 51: 757–763.

Hansen, L. D.; Hopkin, M. S.; Rank, D. R.; Anekonda, T. S.;

Breidenbach, R. W.; Criddle, R. S. 1994. The relationship between

plant growth and respiration: a thermodynamic model. Planta.

194: 77–85.

Hansen, L. D.; Hopkin, M. S.; Criddle, R. S. 1997. Plant calorimetry:

a window to plant physiology and ecology. Thermochimica Acta.

300: 183–197.

Hemming, D. J. B.; Meyer, S. E.; Smith, B. N.; Hansen, L. D. 1999.

Respiration characteristics differ among cheatgrass (Bromus

tectorum L.) populations. Great Basin Naturalist. 59: 355–360.

Klemmedson, J. O.; Smith, J. G. 1964. Cheatgrass (Bromus tectorum L.). The Botanical Review. 30: 226–262.

Mack, R. N.; Pyke, D. A. 1983. The demography of Bromus tectorum: variation in time and space. Journal of Ecology. 71: 69–93.

Mack, R. N.; Pyke, D. A. 1984. The demography of Bromus tectorum:

the role of microclimate, grazing and disease. Journal of Ecology.

72: 731–748.

Meyer, S. E.; Allen, P. S. 1999. Ecological genetics of seed germination regulation in Bromus tectorum L.: I. Phenotypic variance

among and within populations. Oecologia. 120: 27–34.

Morrow, L. A.; Stahlman, P. W. 1984. The history and distribution

of downy brome (Bromus tectorum) in North America. Weed

Science. 32(supplement 1): 2–6.

Nasri, M.; Doescher, P. S. 1995. Effect of competition by cheatgrass

on shoot growth of Idaho fescue. Journal of Range Management.

48: 402–405.

Novak, S. J.; Mack, R. N.; Soltis, D. E. 1991. Genetic variation in

Bromus Tectorum (Poaceae): population differentiation in its

North American Range. American Journal of Botany. 78(8):

1150–1161.

Novak, S. J.; Mack, R. N.; Soltis, P. S. 1993. Genetic variation in

Bromus tectorum(Poaceae): introduction dynamics in North America.

Canadian Journal of Botany. 71: 1441–1448.

Novak, S. J.; Mack, R. N. 1993. Genetic variation in Bromus

tectorum (Poaceae): comparison between native and introduced

populations. Heredity. 71: 167–176.

Richardson, J. M.; Gealy, D. R.; Morrow, L. A. 1989. Influence of

moisture deficits on the reproductive ability of downy brome

(Bromus tectorum). Weed Science. 37: 525–530.

Smith, B. N.; Jones, A. R.; Hansen, L. D. 1999. Growth, respiration

rate, and efficiency responses to temperature. In: Pessarakli, M.,

ed. Handbook of plant and crop stress, 2nd edition. New York:

Marcel Dekker, Inc.: Chapter 18.

Smith, B. N.; Criddle, R. S.; Hansen, L. D. 2000. Plant growth,

respiration and environmental stress. Journal of Plant Biology.

27: 89–97.

Thill, D. C.; Beck, K. G.; Callihan, R. H. 1984. The biology of downy

brome (Bromus tectorum). Weed Science. 32(supplement 1): 7–12.

Upadhyaya, M. K.; Turkington, R.; McIlvride, D. 1986. The biology

of Canadian weeds. 75. Bromus tectorum L. Canadian Journal of

Plant Science. 66: 689–709.

Whisenant, S. G. 1990. Changing fire frequencies on Idaho’s Snake

River plains: ecological and management implications. In:

McArthur, E. D.; Romney, E. M.; Smith, S. D.; Tueller, P. T.,

comps. Proceedings—symposium on cheatgrass invasion, shrub

die-off, and other aspects of shrub biology and management. Gen.

Tech. Rep. INT-276. Ogden, UT: U.S. Department of Agriculture,

Forest Service, Intermountain Research Station: 4–10.
276 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Bruce N. Smith is a Professor, Jillian L. Walker and Rebekka L. Stone are

Undergraduate Students, and Angela R. Jones is a Graduate Student,

Department of Botany and Range Science; Lee D. Hansen is a Professor,

Department of Chemistry and Biochemistry, Brigham Young University,

Provo, UT 84602.

Abstract—Shoots from 4- to 6-day old seedlings of seven ancestral

or old cultivars of Zea mays L. were placed in a calorimeter. Dark

metabolic heat rate (q) and CO2 production rate (RCO2) were measured at nine temperatures (5, 10, 15, 20, 25, 30, 35, 40, and 45 °C).

Temperature dependencies of q and RCO2 were used to model

response of both growth and substrate carbon conversion efficiency.

Responses at 5 °C were similar, but differences were noted at

warmer temperatures. Upper temperature limits for growth were:

Minipopcorn (26 °C), Black popcorn (30 °C), Black Mexican Sweet

(31 °C), Pula Janku (32 °C), Santo Domingo White (32 °C), Loncho

(39 °C), and Santa Ana Blue (45 °C). This study of seedling metabolism reveals climatic adaptation among cultivars that may prove

beneficial to maize production across the globe.

Maize (Zea mays L.) is an important crop originating in

the Americas, now grown for both biomass and grain production in a variety of climatic conditions around the world.

Because small differences in climatic temperature significantly affect maize growth, increased production could result from a better understanding of the effects of temperature on metabolism and growth (Bandolini and others 2000;

Greaves 1996; Miedema 1982; Singletary and others 1994).

All life depends on photosynthesis, however despite much

effort to correlate photosynthesis with growth rates, no

meaningful results have been obtained, only correlations

(Nelson 1988). Respiratory rates of plants have frequently

been empirically correlated with growth rates (Amthor 1989;

Hay and Walker 1989; Loomis and Amthor 1999; Thornley

and Cannell 2000), and a recent model allows predictions of

growth rates from metabolic rate measurements. This

model and rapid methods for measurement allow definition

of responses to subtle changes in environmental factors,

including temperature (Hansen and others 1994).

In an earlier study of maize (Taylor and others 1998), seed

was purchased from commercial sources for nine cultivars of

both flint and dent varieties, and five newer cultivars were

Temperature-Dependent Respiration-Growth

Relations in Ancestral Maize Cultivars

Bruce N. Smith

Jillian L. Walker

Rebekka L. Stone

Angela R. Jones

Lee D. Hansen

supplied by Pioneer Hi-bred International. Metabolic heat

rates and CO2 rates were measured at just two temperatures, and these values were used to model the temperature

dependences of both growth and substrate carbon conversion efficiency (Taylor and others 1998). Some cultivars

were found to grow better at low temperatures, while others

were better at higher temperatures.

For this study we obtained ancestral or old cultivars of

maize and made metabolic measurements at nine temperatures (from 5 to 45 °C at 5 °C intervals) so that the curves

presented are measured rather than calculated.

Respiration has two aspects: catabolism and anabolism.

In catabolism organic substrates are oxidized to produce

CO2. Part of the energy produced by oxidation is used to

convert ADP and inorganic phosphate to ATP, the rest is lost

as heat.

substrate + O2 → CO2 + H2O + ATP + heat (1)

ATP produced in catabolism is transient, but is used for

cellular work, including anabolism as shown below:

substrate + ATP → growth + heat (2)

In anabolism, heat and new plant tissue are produced. A

calorimeter measures the rate of heat loss from both catabolism and anabolism (q). The rate of CO2 production measures the rate of catabolism (RCO2).

Materials and Methods ___________

The specific predicted growth rate of structural biomass or

rate of anabolism (RSG) is related to the two measured

variables as in equation (3).

RSG∆HB = 455RCO2 – q (3)

where ∆HB is the enthalpy change for the formation of

biomass from photosynthate and Thornton’s constant (–455 ±

15 kJ mol–1 of O2) is incorporated.

Seven ancestral or older cultivars of Zea mays L. were

obtained (table 1). (After considerable searching in library

and web sites, we conclude that the experts disagree as to

which cultivars resemble old or ancestral types). Seeds were

germinated at room temperature and about 100 mg fresh

weight of shoot tissue from 4- to 6-day old seedlings was

placed in each of three ampules of the calorimeter (Hart

Scientific model 7707 or Calorimetry Sciences Corporation

MCDSC model 4100). After 15 to 20 minutes thermal

equilibration at the desired temperature, the metabolic
USDA Forest Service Proceedings RMRS-P-21. 2001 277

Temperature-Dependent Respiration-Growth Relations in Ancestral Maize Cultivars Smith, Walker, Stone, Jones, and Hansen

heat rate (q) was measured for another 15 to 20 minutes. The

ampules were removed from the calorimeter and a small vial

filled with 40 μl of 0.4 M NaOH was placed in the calorimeter

ampule with the tissue. Again a 15 to 20 minute thermal

equilibration was necessary, followed by measurement of

Table 1—Maize seedlings were grown from seven ancestral cultivars.

Metabolic heat rate and CO2 rate were measured every 5 °C

from 5 to 45 °C. Low and high stress temperatures are

indicated as well as the temperature for optimal growth.

Temperature response

Cultivar Low stress Optimal High stress

Minipopcorn <5 20 26

Black popcorn <5 20 30

Black Mexican sweet <5 25 31

Pula Janku <5 20 32

Santo Domingo white <5 20 32

Loncho <5 25 39

Santa Ana Blue <5 25 45

Figure 1—(A) Metabolic heat rate (q) and respiration rate (455RCO2) for the Minipopcorn cultivar

of Zea mays L. was measured as μW per mg dry

wt. at 5 degree intervals from 5 to 45 °C. (B)

Predicted specific growth rate (RSG∆HB) was

calculated from the metabolic measurements in

(A) according to equation 3.

the respiration rate (RCO2) for 15 to 20 minutes. As the CO2

and NaOH react in solution, additional heat is produced

(–108.5 kJ mol-1 is the heat of reaction for carbonate formation), giving the rate of CO2 evolution (RCO2) by the plant

tissue. Next the NaOH is removed and the heat rate (q) is

measured as before (Hansen and others 1994; Criddle and

Hansen 1999). The tissue was then run at another temperature. Measurements were made on each sample at 9 temperatures: 5, 10, 15, 20, 25, 30, 35, 40, and 45 °C. Three

samples were used in each of the sequences: 15, 10, and 5 °C;

20, 25, and 30 °C; and 35, 40, and 45 °C.

Results and Discussion __________

For Minipopcorn (fig. 1), the calculated rate of energy

production from catabolism (455RCO2) exceeded heat loss (q)

at 5 through 26 °C, while at higher temperatures heat loss

exceeded calculated energy available from oxidation of

carbohydrate. Above 35 °C, heat rate declined with increasing temperature, indicating possible tissue damage. Thus,

growth (RSG∆HB) was predicted to occur only at temperatures below about 26 °C. By contrast, the data on Black

Popcorn indicated growth would continue up to about 30 °C

(fig. 2), but not at higher temperatures. The calculated

Figure 2—As in figure 1 but for the Black Popcorn cultivar.
278 USDA Forest Service Proceedings RMRS-P-21. 2001

Smith, Walker, Stone, Jones, and Hansen Temperature-Dependent Respiration-Growth Relations in Ancestral Maize Cultivars

Figure 3—As in figure 1 but for the

Black Mexican Sweet cultivar.

Figure 4—As in figure 1 but for the Pula

Janku cultivar.

growth rate of Black Mexican Sweet (fig. 3) had a temperature response a bit higher, to 31 °C. Pulu Janku (fig. 4) and

Santo Domingo White (fig. 5) had very similar responses (to

32 °C). Loncho (fig. 6) was predicted to grow at temperatures

below about 39 °C, while Santa Ana Blue (fig. 7) did well in

warmer temperatures and would grow up to a temperature

of about 45 °C.

Figure 5—As in figure 1 but for the

Santo Domingo White cultivar.

Figure 6—As in figure 1 but for the

Loncho cultivar.
USDA Forest Service Proceedings RMRS-P-21. 2001 279

Temperature-Dependent Respiration-Growth Relations in Ancestral Maize Cultivars Smith, Walker, Stone, Jones, and Hansen

Conclusions____________________

• We studied older corn cultivars, however the experts

disagree as to which cultivars resemble “old” or “ancestral” varieties. Metabolic measurements made in this

and a previous study (Taylor and others 1998) indicate

that the 21 cultivars examined have many similarities,

and perhaps a common origin.

• Some cultivars are adapted to warm climates. Others

are adapted to cooler climates.

• Data obtained from measurements at nine temperatures agrees with that obtained from modelling data at

two temperatures, for example, Taylor and others 1998.

• With climatic information and calorimetric measurements, it is possible to quickly select the best cultivar for

growth in a given location.

References _____________________

Amthor, J. S. 1989. Respiration and crop productivity. New York:

Springer-Verlag.

Brandolini, A.; Landi, P.; Monfredini, G.; Tano, F. 2000. Variation

among Andean races of maize for cold tolerance during heterotrophic and early autotrophic growth. Euphytica. 111: 33–41.

Criddle, R. S.; Hansen, L. D. 1999. Calorimetric methods for analysis of plant metabolism. In: Kemp, R. B., ed. Handbook of thermal

analysis and calorimetry. Vol. 4. Amsterdam: Elsevier: 711–763.

Greaves, J. A. 1996. Improving sub optimal temperature tolerance

in maize—the search for variation. Journal of Experimental

Botany. 47: 307–323.

Hansen, L. D.; Hopkin, M. S.; Rank, D. R.; Anekonda, T. S.;

Breidenbach, R. W.; Criddle, R. S. 1994. The relation between

plant growth and respiration: a thermodynamic model. Planta.

194: 77–85.

Hay, R. K. M.; Walker, A. J. 1989. An introduction to the physiology

of crop yield. Essex: Longman Scientific and Technical: 87–106.

Loomis, R. S.; Amthor, J. S. 1999. Yield potential, plant assimilatory

capacity, and metabolic efficiencies. Crop Science. 39: 1584–1596.

Miedema, P. 1982. The effects of low temperature on Zea mays.

Advances in Agronomy. 35: 93–128.

Nelson, C. J. 1988. Genetic associations between photosynthetic

characteristics and yield: review of the evidence. Plant Physiology and Biochemistry. 26: 543–556.

Singletary, G. W.; Banisadr, R.; Keeling, P. L. 1994. Heat stress

during grain filling in maize: effects on carbohydrate storage

and metabolism. Australian Journal of Plant Physiology. 21:

829–841.

Taylor, D. K.; Rank, D. R.; Keiser, D. R.; Smith, B. N.; Criddle, R. S.;

Hansen, L. D. 1998. Modelling temperature effects on growthrespiration relations of maize. Plant, Cell and Environment. 21:

1143–-1151.

Thornley, J. H. M.; Cannell, M. G. R. 2000. Modelling the components of plant respiration: representation and realism. Annals of

Botany. 85: 55–67.

Figure 7—As in figure 1 but for the Santa Ana Blue

cultivar.

Although no common cultivars were used in this and a

previous study (Taylor and others 1998), the results show

many similarities. Data obtained from metabolic measurements at nine temperatures is more definitive, and in essential agreement with the curves calculated from data at two

temperatures, for example, Taylor and others 1998.

Different responses to temperature by cultivars (table 1)

probably represents adaptation to different climates. All of

the cultivars, except perhaps Black Mexican Sweet, exhibit

a maximum in the calculated growth rate near 20 °C.

Growth rates tend to decline at both higher and lower

temperatures. The anomalous point at 5 °C for Santa Ana

Blue is probably caused by tissue damage from chilling

sensitivity in this cultivar.
280 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Dorothy A. Stradling and Tonya Thygerson are Undergraduate Students;

Bruce N. Smith is a Professor, Department of Botany and Range Science; Lee

D. Hansen and Richard S. Criddle are Professors, Department of Chemistry

and Biochemistry, Brigham Young University, Provo, UT 84602. Rosemary L.

Pendleton is a Project Leader, USDA Forest Service, Rocky Mountain Research Station, Forestry Sciences Laboratory, 2205 Columbia SE, Albuquerque, NM 87106.

Abstract—Cryptogamic crusts are communities composed of lichens, cyanobacteria, algae, mosses, and fungi. These integrated

soil crusts are susceptible to disturbance, but if intact, appear to

play a role in providing nutrients, especially nitrogen, to higher

plants. It is not known how or under what conditions desert crusts

can grow. Crust samples from localities on the Colorado Plateau and

the Great Basin were brought to the laboratory and exposed to

atmospheres of different humidity and different levels of liquid

water. Both metabolic heat rate (q) and carbon dioxide evolution

rate (RCO2) were measured in microcalorimeters at temperatures

from 10 to 35 °C. While exposure to water vapor alone had little

effect, addition of liquid water caused a marked increase in metabolic rate and a switch from anaerobic to aerobic metabolism.

Cryptogamic soil crusts cover as much as 40 to 60 percent

of desert surfaces in the Intermountain Western U.S.A.

(Evans and Johansen 1999). These microbiotic crusts are a

mixture of lichens, mosses, cyanobacteria, and green algae

that retain soil moisture, fix nitrogen, and protect the desert

ecosystem by preceding vascular plant growth and preventing erosion (Brotherson and Rushforth 1983). Grazing by

cattle is most destructive in spring and summer months,

but even in the winter there is a 50 percent reduction in

crusted area compared to a control plot (Memmott and

others 1998). Crusts are vulnerable to destruction by roaming cattle and hikers (Anderson and others 1982). Crusts

play an important role in nitrogen fixation (Evans and

Belnap 1999). They may also be important for making other

essential elements available to higher plants (Harper and

Pendleton 1993).

Aerobic respiration has two aspects: catabolism and anabolism. In catabolism, organic substrates are oxidized to produce CO2 and energy. Part of the energy produced by

Calorimetric Studies of Cryptogamic Crust

Metabolism in Response to Temperature,

Water Vapor, and Liquid Water

Dorothy A. Stradling

Tonya Thygerson

Bruce N. Smith

Lee D. Hansen

Richard S. Criddle

Rosemary L. Pendleton

oxidation is used to convert ADP and inorganic phosphate to

ATP, the rest is lost as heat.

substrate + O2 + ADP + Pi → CO2 + H2O + ATP + heat (1)

ATP produced in catabolism is transient, but is used for

cellular work, including anabolism as shown below:

substrate + ATP→ growth + ADP + Pi

 + heat (2)

In anabolism, heat and new plant tissue are produced and

ATP is hydrolyzed back to ADP and phosphate. A calorimeter measures the rate of heat loss (q) from both catabolism

and anabolism. The rate of CO2 production (RCO2) measures

the rate of catabolism. With carbohydrate as the specific

substrate, predicted growth rate of structural biomass or

rate of anabolism (RSG) is related to three measurable

variables and one constant as in equation 3.

RSG∆HB = 455RCO2 – q (3)

∆HB is the enthalpy change for the formation of biomass

from photosynthate and Thornton’s constant (455 ± 15 kJ

mol–1 of O2) is incorporated to calculate the rate of energy

generated by catabolism. Thus, growth rate in terms of

energy (in other words, RSG∆HB) is proportional to the

difference between the measured values of RCO2 and q. The

temperature dependencies of RCO2 and q are different

(Taylor and others 1998). The difference between 455RCO2

and q therefore changes with temperature and this difference can be used to predict growth rate changes with temperature (Criddle and others 1997).

Predicted specific growth rate may also be expressed as a

function of the substrate carbon conversion efficiency (ε) and

respiration rate (RCO2).

RSG = RCO2[ε/(1–ε)] (4)

Combining equations 3 and 4 to eliminate RSG gives equation 5

q/RCO2 = (1–γP/4)455 – [ε/(1–ε)]∆HB (5)

which relates the ratio of q/RCO2 to ε. Values of q/RCO2

measured as a function of temperature can thus provide

information on substrate carbon conversion efficiency (ε)

and the oxidation state of the substrate carbon, γP (Hansen

and others 1994).

Anaerobic respiration by definition does not involve oxygen uptake and conserves much less of the available energy
USDA Forest Service Proceedings RMRS-P-21. 2001 281

Calorimetric Studies of Cryptogamic Crust Metabolism in Response to Temperature, ... Stradling, Thygerson, Smith, Hansen, Criddle, and Pendleton

than does aerobic catabolism. For this reason, most organisms use oxidative metabolism whenever possible. Anaerobic respiration is immediately recognizable from measurements of q and RCO2 because it produces CO2 but little or no

heat compared to aerobic respiration.

In this study, calorimetry was used to determine the high

and low stress temperatures for desert crust under controlled conditions. When the metabolic heat rate exceeds

energy made available through catabolism of carbohydrate,

the plant is considered to be stressed (Smith and others

2000).

Given their importance, more needs to be learned about

recovery of disturbed crusts (Belnap 1993). Our research

explores conditions of temperature and moisture for optimal growth of microbiotic crust communities. Such information could help land managers protect the crusts during

critical growth periods. In addition, the findings could help

establish better inoculation techniques.

Materials and Methods ___________

Samples were collected near Nephi, Utah, during the fall

and winter of 1999. The cryptogams grew in a sagebrush

community occasionally grazed by cattle. The collected crusts

were approximately 2 cm thick and 15 cm in diameter. They

were collected in petri dishes so the integrity of the crust

could be maintained. No moisture was added at the time of

collection. Samples were subdivided into two sets, one to

measure the effects of humidity and the other to measure the

effects of different amounts of liquid water.

Saturated salt solutions were used to adjust the relative

humidity of the air surrounding crust samples in sealed jars

to 31, 52, 79, and 100 percent, followed by 30 days of

equilibration. A sample with no water or solution added to

the jar was labeled 0 percent humidity and used as a control.

The amount of water taken up was measured by weighing

the crust before and after the equilibration period. In a

separate experiment, different amounts of distilled water

were added to the crust samples two hours preceding the

calorimetric measurements. Following this preparation, the

samples were cut off at the base of the mat and excess soil

removed. Approximately 500 mg of visually equivalent crust

was added to each calorimeter ampule. Measurements of

metabolic heat rate and the rate of carbon dioxide evolution

were taken in the isothermal mode in a Calorimetry Sciences

Corp. Model 4100 calorimeter at 10, 15, 20, 25, and 30 °C.

Results and Discussion __________

Increasing relative humidity up to 100 percent had no

effect on crusts. Heat rates (q) ranged from +0.068 to –0.045

and CO2 rates from 0.614 to 0.031. The ratio of q/RCO2

ranged from +50 to –50 kJ mole–1with an average near

zero. These data demonstrate that anaerobic respiration is

the only important process in crusts exposed to water vapor.

However, addition of even small amounts of liquid water

switches the q/RCO2 ratio to values around 400 kJ mole–1,

very typical of aerobic respiration (Criddle and others 1997;

Hansen and others 1994). Liquid water thus promotes

growth of the crust (fig. 1). This probably relates to the

central role of blue-green algae in metabolism of the desert

crust community. Lange and others (1988) have shown that

lichens with green algal photobionts respond to water

vapor, while lichens with blue-green photobionts respond

only to liquid water. Microtopography of crust growth may

orient the community to maximize water retention (George

and others 2000). The filamentous blue-green algae have a

gelatinous coating which, in the absence of liquid water,

may prevent oxygen uptake and carbon dioxide production,

and thus inhibit oxidative catabolism (Lange and others

1998).

Cryptogamic crusts with added liquid water had a slight,

but not significant, decrease in metabolic efficiency with

increasing temperatures (fig. 2). Thus rather than growing

at a certain season of the year, cryptogamic crusts may show

an opportunistic growth response to a significant rainfall

event at any temperature from 10 to 35 °C.

Figure 2—Cryptogamic crust metabolic efficiency

of carbon conversion, q/RCO2 (kJ mol–1), in response

to temperature, °C.

Figure 1—Cryptogamic crust predicted growth rate,

RSG∆HB (μW/mg dry weight), in response to addition of

liquid water (mg H2

O/ mg dry weight).
282 USDA Forest Service Proceedings RMRS-P-21. 2001

Stradling, Thygerson, Smith, Hansen, Criddle, and Pendleton Calorimetric Studies of Cryptogamic Crust Metabolism in Response to Temperature, ...

Conclusions____________________

• Changing the relative humidity of the air does not affect

metabolism.

• Liquid water is a necessity for cryptogamic crusts to grow.

• Temperature seems to have no effect on either carbon

conversion efficiency or growth rates.

• Growth of cryptogamic crusts is regulated by availability of liquid water rather than by temperature.

References _____________________

Anderson, D. C.; Harper, K. T.; Rushforth, S. R. 1982. Recovery of

cryptogamic soil crusts from grazing on Utah winter ranges.

Journal of Range Management. 35: 355–359.

Belnap, J. 1993. Recovery rates of cryptobiotic crusts: inoculant use

and assessment methods. Great Basin Naturalist. 53: 89–95.

Brotherson, J. D.; Rushforth, S. R. 1983. Influence of cryptogamic

crusts on moisture relationships of soils in Navajo National

Monument, Arizona. Great Basin Naturalist. 43: 73–78.

Criddle, R. S.; Smith, B. N.; Hansen, L. D. 1997. A respiration based

description of plant growth rate responses to temperature. Planta.

201: 441–445.

Evans, R. D.; Belnap, J. 1999. Long-term consequences of disturbance on nitrogen dynamics in an arid ecosystem. Ecology. 80:

150–160.

Evans, R. D.; Johansen, J. R. 1999. Microbiotic crusts and ecosystem

processes. Critical Reviews in Plant Sciences. 18: 183–225.

George, D. B.; Davidson, D. W.; Schliep, K. C.; Patrell-Kim, L. J.

2000. Microtopography of microbiotic crusts on the Colorado

plateau, and distribution of component organisms. Western North

American Naturalist. 60: 343–354.

Hansen, L. D.; Hopkin, M. S.; Rank, E. R.; Anekonda, T. S.;

Breidenbach, R. W.; Criddle, R. S. 1994. The relation between

plant growth and respiration: a thermodynamic model. Planta.

194: 77–85.

Harper, K. T.; Pendleton, R. L. 1993. Cyanobacteria and cyanolichens:

can they enhance availability of essential minerals for higher

plants? Great Basin Naturalist. 53: 59–72.

Lange, O. L.; Belnap, J.; Reichenberger, H. 1998. Photosynthesis of

the cyanobacterial soil-crust lichen Collema tenax from arid

lands in southern Utah, USA: role of water content on light and

temperature responses of CO2 exchange. Functional Ecology. 12:

195–202.

Lange, O. L.; Green, T. G. A.; Ziegler, H. 1988. Water status related

photosynthesis and carbon isotope discrimination in species of

the lichen genus Pseudocyphellaria with green or blue-green

photobionts and in photosymbiodemes. Oecologia. 75: 494–501.

Memmott, K. L.; Anderson, V. J.; Monsen, S. B. 1998. Seasonal

grazing impact on cryptogamic crusts in a cold desert ecosystem.

Journal of Range Management. 51: 547–550.

Smith, B. N.; Criddle, R. S.; Hansen, L. D. 2000. Plant growth,

respiration and environmental stress. Journal of Plant Biology.

27: 89–97.

Taylor, D. K.; Rank, D. R.; Keiser, D. R.; Smith, B. N.; Criddle, R. S.;

Hansen, L. D. 1998. Modeling temperature effects on growthrespiration relations of maize. Plant, Cell and Environment. 21:

1143–1151.
USDA Forest Service Proceedings RMRS-P-21. 2001 283

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Tonya Thygerson and Jennifer M. Harris are Undergraduate Students;

D. Terrance Booth is a Senior Scientist, USDA-ARS, High Plains Grassland

Research Station, Cheyenne, WY 82009. Lee D. Hansen is a Professor,

Department of Chemistry and Biochemistry; Bruce N. Smith is a Professor,

Department of Botany and Range Science, Brigham Young University,

Provo, UT 84602.

Abstract–Eurotia lanata (Pursh) Moq. (winterfat) is a boreal

cold-desert subshrub, seldom more than 2 feet tall, that thrives in

dry climates at cool temperatures. Diaspore collections from

Matador, Saskatchewan, Canada; Pine Bluffs, Wyoming; and

Sterling, Colorado, were cleaned and placed on moistened filter

paper in petri dishes maintained at 0, 5, 10, 15, and 20 °C to study

germination. Seeds germinated at all temperatures but seedlings

were not acclimated to cold by germination temperature. At

radicle emergence (ca. 3 mm), seeds were placed in calorimeter

ampules. Heat-rate (q) was measured at a given temperature,

then a vial containing NaOH solution was added to measure the

rate of CO2 evolution (RCO2) for the same tissue at the same

temperature. This procedure was repeated for each of the populations at temperatures ranging from –10 to +20 °C. Metabolic

efficiency and predicted specific growth rates were calculated

from these measurements. Optimum temperature for germination, metabolism, and early seedling growth was about 10 °C.

Stress was noted near 20 and –5 °C. Acclimation during germination had no effect. Differences between the three populations

correlated with altitude rather than latitude.

Winterfat is a small cold-desert subshrub that thrives in

dry climates at cool temperatures. Stems, leaves, and dispersal units called diaspores are covered with a dense mix of

short and long white hairs that aid in water retention (Booth

and Haferkamp 1995). Foliage and fruit are retained throughout the winter. Winterfat is excellent forage for both wildlife

and domestic cattle and is a good source of protein and

vitamin A. In North America, winterfat is found from Canada

to Mexico, and from Manitoba to British Columbia and the

Dakotas and Nebraska west to the Great Basin. The genus

consists of only two species, one from North America, the

other from the cold deserts of Asia (Mozingo 1987).

Microcalorimetric Studies on Metabolic and

Germination Response to Temperature for

Three Populations of Winterfat (Eurotia

lanata)

Tonya Thygerson

D. Terrance Booth

Jennifer M. Harris

Lee D. Hansen

Bruce N. Smith

Populations within a species (accessions) are adapted to

the particular microclimate of their origin and usually do not

grow well when moved to a slightly different location. The

purpose of this work is to examine how plants adapt their

respiratory metabolism to match the temperature of their

native climate. In this study, calorimetry was used to determine the temperature response and high and low stress

temperatures of winterfat diaspores collected from three

locations. When metabolic heat loss exceeds energy made

available through catabolism of carbohydrate, the plant is

considered to be stressed (Smith and others 2000).

Aerobic respiration has two aspects: catabolism and

anabolism. In catabolism, organic substrates are oxidized

to produce CO2. Part of the energy produced by oxidation is

used to convert ADP and inorganic phosphate to ATP, the

rest is lost as heat.

substrate + O2 + ADP + Pi → CO2 + H2O + ATP + heat (1)

ATP produced in catabolism is transient, but is used for

cellular work, including anabolism as shown below:

substrate + ATP → growth + ADP + Pi

 + heat (2)

In anabolism, heat and new plant tissue are produced and

ATP is hydrolyzed back to ADP and phosphate. A calorimeter measures the rate of heat loss (q) from both catabolism

and anabolism. The rate of CO2 production (RCO2) measures the rate of catabolism. With carbohydrate as the

specific substrate, predicted growth rate of structural biomass or rate of anabolism (RSG) is related to the two

measured variables as in equation 3.

RSG∆HB = 455RCO2 – q (3)

where ∆HB is the enthalpy change for the formation of

biomass from photosynthate and Thornton’s constant (–455 ±

15 kJ mol–1 of O2) is incorporated to calculate the rate of

energy generated by catabolism. Thus, growth rate in terms

of energy is proportional to the difference between the

measured values of RCO2 and q. The temperature dependencies of RCO2 and q are different (Hansen and others

1994). The difference between 455RCO2 and q therefore

changes with temperature and this difference can be used

to predict growth rate changes with temperature (Criddle

and others 1997).
284 USDA Forest Service Proceedings RMRS-P-21. 2001

Thygerson, Booth, Harris, Hansen, and Smith Microcalorimetric Studies on Metabolic and Germination Response to Temperature ...

Predicted specific growth rate may also be expressed as a

function of the substrate carbon conversion efficiency (ε) and

respiration rate (RCO2).

RSG = RCO2 [ε/(1–ε)] (4)

Combining equations 3 and 4 to eliminate RSG gives equation 5

(ε/1–ε)∆HB = –q/RCO2 – (1–γP/4)455 (5)

which relates the ratio of q/RCO2 to ε. Values of q/RCO2

measured as a function of temperature can thus provide

information on substrate carbon conversion efficiency (ε)

and the oxidation state of the substrate carbon, γP (Hansen

and others 1994).

Winterfat diaspores collected from three locations were

compared at several temperatures using calorimetry.

Materials and Methods ___________

Diaspores from Eurotia lanata (Pursh) Moq. (winterfat)

were collected from Matador, Saskatchewan, Canada; Pine

Bluffs, Wyoming; and Sterling, Colorado (table 1; Bai and

others 1999). The diaspore was first removed from the

seed to decrease fungal growth during germination (Booth

and Haferkamp 1995). The threshed seeds were soaked in

a tween solution (10 percent) for 10 minutes, then in

dilute sodium hypochlorite (1 percent) for 45 minutes.

Then the seeds were placed on moistened filter paper in

petri dishes kept in beakers partially submerged in coolant baths maintained at 0, 5, 10, 15, and 20 °C to study

acclimation effects on germination and metabolism.

At the time of radicle emergence (to about 3 mm), seeds

(about 100 mg fresh weight) were placed in each of three

ampules of a microcalorimeter (Hart Scientific model 7707

or Calorimetry Sciences Corporation MCDSC model 4100).

After 15 to 20 minutes thermal equilibration at the desired

temperature, the metabolic heat rate (q) was measured for

another 15 to 20 minutes. The ampules were removed from

the calorimeter and a small vial filled with 40 μl of 0.4 M

NaOH placed in the calorimeter ampule with the tissue.

Again a 15 to 20 minute thermal equilibration was necessary, followed by measurement of the sum of the heat from

metabolism and CO2 reaction with the NaOH for 15 to 20

minutes. After the NaOH is removed the heat rate (q) is

measured again as before (Hansen and others 1994; Criddle

and others 1997). The reaction of CO2 with the NaOH

solution to form carbonate produces –108.5 kJ mol–1.

Dividing the difference in the measurements with and

without NaOH solution present gives the rate of CO2

evolution (RCO2) by the plant tissue. The tissue was then run

at another temperature. Measurements were made on each

sample at 7 temperatures: 20, 15, 10, 5, 0, –5, and –10 °C.

Results and Discussion __________

Acclimating germinating seeds at various temperatures

had no effect on germination or metabolism. Seeds germinated as rapidly at 0 °C as they did at 20 °C with essentially

100 percent germination at all temperatures in agreement

with previous work (Bai and others 1998a). Also seeds

germinated at a given temperature, say 5 °C, showed no

different metabolic response at 5 °C than did seeds germinated at 15 °C (Bai and others 1998b). Desiccation and cold

hardiness are often linked in winterfat (Hou and others

1999).

Since growth in terms of energy can occur only when

catabolic energy generation rate (455RCO2) exceeds total

heat loss (q), metabolic data (fig. 1) for the winterfat

population from Pinebluffs, Wyoming, indicated cold stress

near 0 °C and heat stress at about 18 °C. Please note that

a smaller ratio of q/RCO2 indicates greater efficiency (fig. 2)

with values greater than 455 μW mg–1 dry wt. representing

Table 1—Sources and habitats for winterfat seeds (after Bai and others 1999).

Seed weight

Site Location Community g/100 seeds

Pine Bluffs, Wyoming, U.S.A. 41°10’N, 104°09’W mixed prairie 0.18

elevation 1554 m

Sterling, Colorado, U.S.A. 40°37’N, 103°13’W shortgrass prairie 0.23

elevation 1181 m

Matador, Saskatchewan, Canada 50°42’N, 107°43’W mixed prairie 0.25

elevation 685 m

Figure 1—Winterfat seedlings from Pinebluffs, Wyoming, U.S.A.; metabolic heat rate (q), ( ), and respiration rate (455RCO2), (o), as μW per mg dry wt. versus

temperature measured at 5 °C intervals.
USDA Forest Service Proceedings RMRS-P-21. 2001 285

Microcalorimetric Studies on Metabolic and Germination Response to Temperature... Thygerson, Booth, Harris, Hansen, and Smith

Figure 4—Winterfat seedlings from Sterling, Colorado,

U.S.A., as in figure 1.

Figure 5—Winterfat seedlings from Matador,

Saskatchewan, Canada, as in figure 1.

a shift to another substrate (for example, lipid) or physical

damage. Negative points in figure 3 occur because the

substrate was assumed to be carbohydrate. Relative specific

growth rates (RSG) less than zero occur then this assumption

is invalid.

Winterfat seedlings from Sterling, Colorado, (fig. 4) were

cold-stressed at about –8 °C and heat stressed at about 16 °C

with good efficiency (fig. 2) and growth (fig. 3) predicted

between those temperatures.

Seedlings from Matador, Saskatchewan, Canada, (fig. 5)

were cold-stressed at about –6 °C and heat stressed at about

19 °C with maximum efficiency (fig. 2) and growth (fig. 3)

between 8 and 12 °C.

Seed weights decreased (Bai and others 1999) with increasing elevation (table 1). The highest elevation site probably has the shortest growing season. However, once daytime temperatures are above freezing, rapid growth can

occur. Note that the Pinebluffs’ population (figs. 1, 2, and 5)

Figure 3—Comparison of the predicted growth rate

(RSG∆HB in μW/mg) of the three populations versus

temperature. Pinebluffs ( ), Sterling (o), and Matador

(❷). RSG∆HB values lower than zero indicate temperatures where no growth occurs.

Figure 2—Comparison of the metabolic efficiency (q/RCO2

in kJ/mole) of the three populations versus temperature.

Pinebluffs ( ), Sterling (o), and Matador (❷). Note: smaller

numbers mean greater efficiency.
286 USDA Forest Service Proceedings RMRS-P-21. 2001

Thygerson, Booth, Harris, Hansen, and Smith Microcalorimetric Studies on Metabolic and Germination Response to Temperature ...

has a more narrow temperature range for growth, but

efficiency of carbon conversion and growth rate exceeds

those of both of the other populations. Metabolic data presented here indicate that these three closely related populations are differently adapted to temperature at their

respective sites. We plan to expand this study to include

winterfat populations across a broader range of environments. This may allow us to determine if the differences

noted here among seedling populations also persist for

mature plants grown in situ or in common gardens.

Conclusions____________________

• Optimum temperature for metabolism and early seedling growth for three populations of winterfat is about

10 °C. Stress is noted below –5 and above +20 °C.

• Metabolic differences among the three populations studied were correlated with altitude rather than latitude,

and probably reflect adaptation to different thermal

environments.

• Winterfat seeds imbibe water, germinate, and grow at

very cool temperatures—even 0 °C. Acclimation had no

effect. Thus seeds germinated at 5 °C did no better at

that temperature than did seeds germinated at 20 °C.

References _____________________

Bai, Y.; Booth, D. T.; Romo, J. T. 1998a. Winterfat (Eurotia lanata

(Pursh) Moq.) seedbed ecology: low temperature exotherms and

cold hardiness in hydrated seeds as influenced by imbibition

temperature. Annals of Botany. 81: 595–602.

Bai, Y.; Booth, D. T.; Romo, J. T. 1998b. Developmental stages of

winterfat germinants related to survival after freezing. Journal

of Range Management. 51: 709–713.

Bai, Y.; Booth, D. T.; Romo, J. T. 1999. Imbibition temperature affects

winterfat (Eurotia lanata (Pursh) Moq.) seed hydration and coldhardiness response. Journal of Range Management. 52: 271–274.

Booth, D. T.; Haferkamp, M. R. 1995. Morphology and seedling

establishment. In: Bedunah, D. J.; Sosebee, R. E., eds. Wildland

plants: physiological ecology and developmental morphology.

Denver, CO: Society For Range Management: 239–290.

Criddle, R. S.; Smith, B. N.; Hansen, L. D. 1997. A respiration based

description of plant growth rate responses to temperature. Planta.

201: 441–445.

Hansen, L. D.; Hopkin, M. S.; Rank, E. R.; Anekonda, T. S.; Breidenbach,

R. W.; Criddle, R. S. 1994. The relation between plant growth and

respiration: A thermodynamic model. Planta. 194: 77–85.

Hou, J. Q.; Romo, J. T.; Bai Y.; Booth, D. T. 1999. Responses of

winterfat seeds and seedlings to desiccation. Journal of Range

Management. 52: 387–393.

Mozingo, H. N. 1987. Shrubs of the Great Basin. Reno, NV: University of Nevada Press: 67–72.

Smith, B. N.; Criddle, R. S.; Hansen, L. D. 2000. Plant growth,

respiration and environmental stress. Journal of Plant Biology.

27: 89–97.
USDA Forest Service Proceedings RMRS-P-21. 2001 287

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

D. J. Weber is a Professor of Botany, Department of Botany and

Range Science, 683 Widtsoe, Brigham Young University, Provo, UT 84602.

T. Williams, N. Williams, P. Wayman, and S. Warner are Students at

Brigham Young University, Provo, UT 84602. A. Khan is a Professor of

Botany, Department of Botany, University of Karachi, Karachi, Pakistan.

B. Gul is a recent Ph.D. associated with the Department of Botany, University

of Karachi, Karachi, Pakistan.

Abstract—Of the world’s land area, about 7 percent is salt affected.

Irrigated land is more susceptible to salinity and it is estimated that

over 1/3 of the irrigated soils are becoming saline. Certain plants

(halophytes) grow well on high saline soils. One approach would be

to grow halophytes on high saline soils and harvest their seeds. The

oil in the seeds would be extracted for cooking oil. The amount of

unsaturated fatty acids is a measure of the quality of cooking oil.

High-unsaturated fatty acid content is considered a factor in preventing heart diseases. Seeds of seven halophytic shrubs were

extracted and the oil was analyzed for fatty acids using gas chromatography and mass spectrometry. The average unsaturation for the

fatty acids in the seed oil was 84 percent, which is a favorable

percent. The major saturated fatty acid was Hexadecanoic acid.

There were several dominant unsaturated fatty acids namely: 9,12-

Octadecadienoic acid, 13-Octadecenoic acid, 11-Eicosenoic acid,

9,12,15, Octadecatrienoic acid, and 9-Octadecenoic acid. It appears

that these halophytes have potential for reclaiming and utilizing

saline soil.

Introduction ____________________

Approximately 7 percent of the world’s land area is salt

affected (Dudal and Purnell 1986). The Great Basin area of

the Western United States has no river that drains the water

to the sea. The water drains into inland lakes such as Great

Salt Lake or evaporates in the valleys. Many salt playa

accumulate in the Great Basin area. The inland salt playas

are harsh environments for living organisms (Goodin and

others 1990). The high salt content of the soil limits the

plant communities to mainly halophytic plants. This includes salt tolerant shrubs and annuals. The salinity of

the soil ranges from 29 dS/m (2 percent NaCl) to 145 dS/m

Composition of Vegetable Oil From

Seeds of Native Halophytes

D. J. Weber

B. Gul

A. Khan

T. Williams

N. Williams

P. Wayman

S. Warner

(9 percent). The salinity of the soil in the bottom of the salt

pans can be as high as 15 percent salt. At the same time

desert conditions exist during the hot summer months.

Precipitation is about 66 mm (2.6 inches) per year. The water

table varies from 1 m to 3.3 m below the surface (Khan and

Ungar 1995).

Dregne and others (1991) suggested that about 74 million

hectares of land are salt affected due to human causes. For

use in the agricultural area, salt tolerant agriculture plants

have been selected to grow on the saline soils. There has been

some success but the selected agriculture plants cannot

tolerate very high saline conditions. Another approach to

this problem is to grow plants that are adapted to saline soils

such as halophytes and then find an economic value for the

halophytes (Khan and others 1990). One possibility would

be animal forage or fuel (presto logs). The economic return of

these products is low. A more valuable economic product

would be cooking oil. Cooking oil is a basic food need throughout the world. The seeds of halophytes contain oil that could

potentially be extracted for human use.

The composition of cooking oils has an impact on health.

Dietary studies (Hu 1997; Lang 1997) support the concept

that diets that are high in saturated fats result in greater

risk to heart diseases. In contrast, foods that are high in

polyunsaturated fatty acids are considered much more

healthy. Animal fats are high in saturated fatty acids whereas

plant fats are normally high in unsaturated fatty acids. A

saturated fatty acid such as stearic acid has no double bonds

in the hydrocarbon chain. With unsaturated fatty acids such

as oleic acid, there is one double bond in the hydrocarbon

chain. Linoleic has two double bonds and alpha linolenic acid

has three double bonds in the hydrocarbon chain.

The purpose of this investigation was to analyze the oil

from several native halophytes to determine their fatty acid

content and quality.

Methods _______________________

Seeds of native halophytes were collected from salt playa

and salt marsh areas in Utah Valley and Rush Valley in

north-central Utah. The seeds were separated from the

vegetative plant parts and cleaned. The seeds were ground

with a Wiley mill and extracted three times with methanol

and chloroform (1:2 v/v). The percent oil in the seeds was

determined by weight.
288 USDA Forest Service Proceedings RMRS-P-21. 2001

Weber, Gul, Khan, Williams, Williams, Wayman, and Warner Composition of Vegetable Oil From Seeds of Native Halophytes

The fatty acids in the oil extract were methylated with

Alltech meth prep 1 ((trifluoromethylphenyl) trimethylammonium hydroxide). The methylated fatty acids were separated by gas chromatography and identified by GC mass

spectrometry.

Results ________________________

The following salt tolerant plants were analyzed for total

oil content in their seeds and the fatty acids in the seed oil.

Allenrolfea occidentialis (Wats) Kuntze

One of the most salt tolerant plants in the Great Basin

area. It has a fleshy stem with reduced leaves. The oil

content of the seeds was 14 percent. The fatty acid composition was: 88.33 percent unsaturated and 11.67 percent

saturated.

Unsaturated fatty acids Percent of fraction

7-Hexadecenoic acid, methyl ester 0.30

9-Hexadecenoic acid, methyl ester 0.29

9-Octadecenoic acid, methyl ester 24.69

11-Eicosenoic acid, methyl ester 11.89

13-Docosenoic acid, methyl ester 15.13

9,12-Octadecadienoic acid, methyl ester 16.78

10,13-Octadecadienoic acid, methyl ester 23.57

9,12,15, Octadecatrienoic acid, methyl ester 7.36

Saturated fatty acids Percent of fraction

Hexadecanoic acid, methyl ester 45.79

Heptadecanoic acid, methyl ester 2.06

Octadecanoic acid, methyl ester 19.93

Eicosanoic acid, methyl ester 10.92

Docosanoic acid, methyl ester 9.98

Teracosanoic acid, methyl ester 9.56

Pentadecanoic acid, methyl ester 0.68

Oxiraneundecanoic acid, 3 pentyl methyl ester 0.99

Atriplex heterosperma Bunge

This is a two-seeded Atriplex that grows in saline areas.

The oil content of the seeds was 15.8 percent. The fatty acid

composition was: 84.73 percent unsaturated and 15.27 percent saturated.

Unsaturated fatty acids Percent of fraction

9-Hexadecenoic acid, methyl ester 0.61

11-Eicosenoic acid, methyl ester 7.01

13-Docosenoic acid, methyl ester 15.13

13-Octadecenoic acid, methyl ester 75.06

15-Tetracosenoic acid, methyl ester 1.02

6,9-Octadecadienoic acid, methyl ester 0.28

9,12,15, Octadecatrienoic acid, methyl ester 0.89

Saturated fatty acids Percent of fraction

Nonanedioic acid dimethyl ester 2.87

Hexadecanoic acid, methyl ester 69.95

Octadecanoic acid, methyl ester 14.65

Eicosanoic acid, methyl ester 11.32

Teracosanoic acid, methyl ester 1.21

Atriplex rosea L.

This Atriplex grows in disturbed areas and is wide spread

in the world. The oil content of the seeds was 12.9 percent.

The fatty acid composition was: 82.79 percent unsaturated

and 17.21 percent saturated.

Unsaturated fatty acids Percent of fraction

9-Hexadecenoic acid, methyl ester 0.31

9-Octadecenoic acid, methyl ester 5.58

13-Octadecenoic acid, methyl ester 40.50

11-Eicosenoic acid, methyl ester 12.36

13-Docosenoic acid, methyl ester 13.89

15-Tetracosenoic acid, methyl ester 0.35

6.9-Octadecadienoic acid, methyl ester 0.15

7,10-Octadecadienoic acid, methyl ester 0.13

8,11-Octadecadienoic acid, methyl ester 1.21

9,12-Octadecadienoic acid, methyl ester 0.37

9,12,15, Octadecatrienoic acid, methyl ester 25.15

Saturated fatty acids Percent of fraction

Hexadecanoic acid, methyl ester 51.47

Hexadecanoic acid, 14-methyl ester 1.31

Heneicosanoic acid, methyl ester 1.14

Octadioic acid, methyl ester 3.93

Nonanedioic acid, methyl ester 2.11

Octadecanoic acid, methyl ester 11.54

Eicosanoic acid, methyl ester 10.21

Docosanoic acid, methyl ester 3.85

Teracosanoic acid, methyl ester 3.14

15-Teracosanoic acid, methyl ester 5.46

Tricosanoic acid, methyl ester 0.83

Pentadecanoic acid, methyl ester 0.60

Oxiraneundecanoic acid, 3 pentyl methyl ester 1.65

Oxiraneundecanoic acid, 3 octyl methyl ester 2.76

Halogeton glomeratus (Bieb.) C. A. Mey

This plant is a native of Asia and grows well on alkaline

soil. It contains oxalates that can be toxic to livestock if eaten

in excess. The oil content of the seeds was 24.7 percent. The

fatty acid composition was: 84.38 percent unsaturated and

15.62 percent saturated.

Unsaturated fatty acids Percent of fraction

9-Hexadecenoic acid, methyl ester 0.48

Hexadecenoic acid, 14-methyl ester 0.16

13-Octadecenoic acid, methyl ester 66.54

11-Eicosenoic acid, methyl ester 2.44

13-Docosenoic acid, methyl ester 1.27

15-Tetracosenoic acid, methyl ester 0.32

6.9-Octadecadienoic acid, methyl ester 0.15

9,10-Octadecadienoic acid, methyl ester 0.24

7,10-Octadecadienoic acid, methyl ester 0.67

9,11-Octadecadienoic acid, methyl ester 0.28

9,12-Octadecadienoic acid, methyl ester 20.04

9,12,15, Octadecatrienoic acid, methyl ester 7.41

Saturated fatty acids Percent of fraction

Hexadecanoic acid, methyl ester 77.10

Hexacosanoic acid, methyl ester 1.01

Octadecanoic acid, methyl ester 11.56

Eicosanoic acid, methyl ester 4.55
USDA Forest Service Proceedings RMRS-P-21. 2001 289

Composition of Vegetable Oil From Seeds of Native Halophytes Weber, Gul, Khan, Williams, Williams, Wayman, and Warner

Docosanoic acid, methyl ester 3.01

Teracosanoic acid, methyl ester 2.51

Tricosanoic acid, methyl ester 0.26

Kochia scoparia (L.) Schrader

An annual plant that grows on saline soils and can be

grazed by livestock. The oil content of the seeds was 9.7

percent. The fatty acid composition was: 80.79 percent

unsaturated and 19.21 percent saturated.

Unsaturated fatty acids Percent of fraction

9-Hexadecenoic acid, methyl ester 4.43

11-Eicosenoic acid, methyl ester 2.30

13-Docosenoic acid, methyl ester 2.59

15-Tetracosenoic acid, methyl ester 0.83

2,4-Hexadiecendioic acid, methyl ester 0.33

9,12-Octadecadienoic acid, methyl ester 89.52

Saturated fatty acids Percent of fraction

Hexadecanoic acid, methyl ester 68.00

Heptadecosanoic acid, methyl ester 0.61

Hexacosanoic acid, methyl ester 0.88

Octadecanoic acid, methyl ester 16.68

Eicosanoic acid, methyl ester 4.61

Docosanoic acid, methyl ester 3.64

Teracosanoic acid, methyl ester 5.58

Sarcobatus vermiculatus (Hook.) Torr.

A perennial shrub that grows well on saline or alkaline

flood plains. It is moderately poisonous to livestock if eaten

in large amounts. The oil content of the seeds was 17.5

percent. The fatty acid composition was: 78.86 percent

unsaturated and 21.14 percent saturated.

Unsaturated fatty acids Percent of fraction

9-Hexadecenoic acid, methyl ester 0.45

11-Eicosenoic acid, methyl ester 1.22

13-Docosenoic acid, methyl ester 1.26

15-Tetracosenoic acid, methyl ester 0.28

7,10-Octadecadienoic acid, methyl ester 0.34

9,12 Octadecadienoic acid, methyl ester 96.16

Octadecatrienoic acid, methyl ester 0.29

Saturated fatty acids Percent of fraction

Hexadecanoic acid, methyl ester 64.30

Heptadecosanoic acid, methyl ester 1.79

Hexacosanoic acid, methyl ester 1.54

Heneicosanoic acid, methyl ester 2.07

Octadecanoic acid, methyl ester 5.82

Tetradecanoic acid, methyl ester 13.15

Eicosanoic acid, methyl ester 4.96

Docosanoic acid, methyl ester 3.56

Tetracosanoic acid, methyl ester 1.23

Tricosanoic acid, methyl ester 1.49

Suaeda torreyana Wats

A shrubby plant that is commonly associated with salt

desert shrub communities. It produces black and brown

seeds that have different properties towards salinity. The oil

content of the seeds was 25.25 percent.

The fatty acid composition was: 89.58 percent unsaturated

and 10.42 percent saturated.

Unsaturated fatty acids Percent of fraction

9-Hexadecenoic acid, methyl ester 0.39

Hexadecenoic acid, 14-methyl ester 6.94

7-Hexadecenoic acid, 14-methyl ester 0.38

Nonanedioic acid, methyl ester 0.51

11-Eicosenoic acid, methyl ester 1.12

13-Docosenoic acid, methyl ester 2.40

15-Tetracosenoic acid, methyl ester 0.17

7,10-Octadecadienoic acid, methyl ester 0.95

9,12-Octadecadienoic acid, methyl ester 86.21

9,12,15, Octadecatrienoic acid, methyl ester 0.93

Saturated fatty acids Percent of fraction

Hexadecanoic acid, methyl ester 58.27

Hexacosanoic acid, methyl ester 0.73

Heneicosanoic acid, methyl ester 1.86

Octadecanoic acid, methyl ester 19.70

Tetradecanoic acid, methyl ester 0.95

Eicosanoic acid, methyl ester 6.11

Docosanoic acid, methyl ester 6.24

Tetracosanoic acid, methyl ester 6.14

The percent unsaturation for the oil from the seeds of the

halophytes ranges from 78.8 percent to 89.5 percent with an

average of 84.2 percent.

Certain fatty acids tended to represent the major concentration. In the saturated fatty acids fraction of the halophytic seed oil, hexadecanoic acid was the major fatty acid in

all cases. The average percent of the fraction was 62 percent.

In the unsaturated fatty acids, there was more diversity

with 9,12-Octadecadienoic acid being the most common,

followed by 13-Octadecenoic acid, 11-Eicosenoic acid, 9,12,15,

Octadecatrienoic acid, and 9-Octadecenoic acid. The total

number of fatty acids detected for Allenrolfea occidentialis

was 31 even though the concentration of most of the individual fatty acids were very low.

Discussion _____________________

The seeds of the halophytes analyzed had an oil content

ranging from 9.7 percent in Kochiato 25.5 percent in Sueada.

The actual yield per hectare for these halophyes has not been

determined. In the case of the Salicornia europaea, field

studies in Mexico, Egypt, and United Arab Emirates indicated a production of 20 tons of plant material per hectare

(Goodin and others 1990). The oilseed yield was 2 ton per

hectare. Based on 15 percent oil content, the oil yield would

be 600 lbs of cooking oil per hectare (Goodin and others

1990).

The quality of the cooking oil is of importance and is

related to the percent unsaturation. High unsaturation is

considered more healthy. Animal fat (lard) is 59 percent

unsaturated and butter is 32 percent unsaturated. Plant

fats are higher in unsaturated fatty acids such as soybean

(84.6 percent), olive oil (85.8 percent), safflower oil (91.l

percent) and canola oil (92.8 percent) (USDA handbook 8-4).

The percent unsaturated from the seed oil of the halophytes
290 USDA Forest Service Proceedings RMRS-P-21. 2001

Weber, Gul, Khan, Williams, Williams, Wayman, and Warner Composition of Vegetable Oil From Seeds of Native Halophytes

was favorable with the average being 84 percent. The seed

oil of Sueada torreyana had an unsaturation of 89.6 percent,

which is very close to canola oil. These results would suggest

that the oil from the halophyte seeds is of high quality.

Future questions that need to be answered include conditions for establishment of stands of halophytes, level of

production, and yield of seeds.

References _____________________

Dregne, H.; Kassas, M.; Razanov, B. 1991. A new assessment of the

world status of desertification. Desertification Control Bulletin.

United Nations Environment Programme. 20:6–18.

Dudal, R.; Purnell, M.F. 1986. Land resources: salt affected soils.

Reclamation and Revegetation Research. 5:1–10.

Goodin, J.R.; Epstein, E.; McKell, C.M.; O’Leary, J.W. 1990. Saline

agriculture, salt-tolerant plants for developing countries. Washington, DC: National Academy Press. 143 p.

Hu, F. 1997. Dietary fat intake and the risk of coronary heart

disease in women. New England Journal of Medicine.

337:1491–1499.

Khan, M.; Ungar, I.A. 1995. Biology of salt tolerant plants. University of Karachi, Karachi, Pakistan. 419 p.

Lang, L. 1997. Types of dietary fat key to heart risk. Reuters Health

Information Services, Inc.

USDA. 1990. Composition of foods: fats and oils—raw, processed,

prepared. Agric. Handb. 8-4. Beltsville, MD: U.S. Department of

Agriculture.
USDA Forest Service Proceedings RMRS-P-21. 2001 291

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Jerry R. Barrow is a Research Geneticist, USDA-ARS, Jornada Experimental Range, P.O. Box 30003, MSC, 3JER, NMSU, Las Cruces, NM 88003-8003.

Abstract—Mycorrhizal fungi enhance the nutrition and survival of

host plants in native ecosystems. Arid rangelands severely challenge plants because of chronic nutrient and water stress. Fourwing

saltbush, Atriplex canescens (Pursh) Nutt., a dominant and important shrub of western arid rangelands, generally considered to be

non-mycorrhizal, is more extensively colonized by dark septate (DS)

fungal endophytes than by traditional mycorrhizal fungi. Roots of

fourwing saltbush colonized by DS fungi were stained with sudan IV

and analyzed with differential interference microscopy that revealed extensive internal colonization by vacuolated hyaline hyphae that is not evident using conventional fungus staining methods. Fungal vacuoles accumulated substantial quantities of lipids in

the sieve elements and cortex when roots were physiologically

active. The widespread colonization of fourwing saltbush by DS

fungi and their extensive accumulation of lipids suggests that these

fungi transport and manage carbon in arid ecosystems. Their

potential role in ecosystems stability is discussed.

Mycorrhizal fungi form specific internal interfaces by

which they exchange resources with their host. Their hyphae extend from the root into soil enhancing the uptake and

transport of mineral nutrients. They perform varied and

significant ecological functions in native ecosystems such as

enhanced nutrition, water relations and survival of host

plants. They regulate key processes that impact soil, vegetation structure, and stability. Recent evidence suggests that

external hyphae also link plants together within a community, forming a common mycorrhizal network by which

plants may share carbon and mineral nutrients. The transport and sharing of essential resources such as carbon and

mineral nutrients could significantly affect the structure

and stability of native plant communities (Ayling and others

1997; Brandes and others 1998; Duan and others 1996;

Graves and others 1997; Simard and others 1997).

The mycorrhizal status of desert plants is not clearly

defined, but their survival in water and nutrient stressed

arid ecosystems is likely enhanced by mycorrhizal or other

symbiotic fungi. Chenopodiacious shrubs, common in many

arid ecosystems, are generally considered to be non-mycorrhizal (Aguilera and others 1998). Fourwing saltbush,

Atriplex canescens (Pursh) Nutt., is an ubiquitous and ecologically important shrub in arid southwestern U.S.A. rangelands. Its roots are more extensively colonized by dark

Carbon Transport by Symbiotic Fungi in

Fourwing Saltbush, Atriplex canescens

(Pursh) Nutt.

Jerry R. Barrow

septate endophytic fungi (DS) than by traditional mycorrhizal fungi (Barrow and others 1997). DS fungi are widespread root colonizers in many stressed ecosystems. These

fungi form nondestructive interfaces with roots and species

include recognized pathogens, saprophytes, soil and rhizosphere inhabiting fungi (Jumpponen and Trappe 1998). It

has been suggested that they may establish beneficial associations with specific plants under stressed conditions that

are unfavorable for traditional mycorrhizal fungi (Kohn and

Stasovski 1990). DS fungi are typically recognized as stained

or pigmented (melanized) hyphae and microsclerotia in

roots prepared and stained with conventional fungal staining and microscopic methods. Their ubiquitous presence in

stressed ecosystems strongly suggests an important but

presently unresolved ecological function (Jumpponen and

Trappe 1998).

Fungal associations with plants range from parasitic to

mutually beneficial. This relationship is based upon the

costs expended or benefits received by each partner (Smith

and Smith 1996). Mycorrhizal fungi form nondestructive

interfaces with plant roots and supply mineral nutrients in

exchange for organic carbon constituting a mutually beneficial relationship. Mycorrhizal fungi vary in their strategy for

accessing and utilizing carbon (Smith and Read 1998). The

internal mycelia of obligate arbuscular mycorrhizae (AM)

fungi can only assimilate photosynthetically derived glucose

from the host, from which they synthesize lipids, and transfer them to the external mycelia. The external mycellia are

incapable of assimilating glucose or other forms of organic

carbon (Sachar-Hill and others 1995; Pfeffer and others

1999). The external hyphae of ectomycorrhizal fungi are able

to hydrolyze and utilize complex external polysaccharides

(Smith and Read 1998). Ericoid mycorrhizal fungi degrade

cellulose, pectin, and lignin (Cairney and Burke 1998) and

wood rotting orchid mycorrhizal fungi can degrade lignin

and other complex soil organic matter and transfer simple

sugars to the heterotrophic protocorm for growth and differentiation of a shoot and root system (Peterson and others

1998).

Barrow and Aaltonen (2001) analyzed roots of A. canescens

colonized by DS fungi with differential interference microscopy (DIC). They observed extensive nondestructive colonization of the cortex and vascular cylinder with hyaline

hyphae that are not visible with conventional staining and

microscopy. Staining of physiologically active roots with

sudan IV revealed substantial accumulation of lipids in

fungal vacuoles that further enhanced fungal visibility and

suggested that carbon management and transport may be a

significant ecological function of DS fungi. The objective of

this study was to analyze A. canescens roots colonized by DS

fungi at different levels of physiological activity and to
292 USDA Forest Service Proceedings RMRS-P-21. 2001

Barrow Carbon Transport by Symbiotic Fungi in Fourwing Saltbush, Atriplex canescens (Pursh) Nutt.

determine if lipid accumulation is affected by seasonal

influence.

Materials and Methods ___________

Roots were sampled from a native population of A. canescens

near the headquarters of the USDA Agricultural Research

Service’s Jornada Experimental Range in southern New

Mexico from winter, early to late spring, summer, until late

fall of 1999. They were prepared and cleared using modified

methods developed by Bevege (1969), Brundrett and others

(1983), Kormanik and others (1980), and Phillips and Hayman

(1970) for A. canescens roots. They were stained with sudan

IV and analyzed with DIC microscopy using the method

developed by Barrow and Aaltonen (2001).

Results ________________________

The expression of DS fungal colonization in A. canescens

roots was highly variable and was affected by the conditions

of the plant or soil at the time of sampling. Typical DS fungal

structures, pigmented (melanized) septate hyphae, and

microsclerotia, were most frequently observed within the

cortex of physiologically inactive roots sampled during the

winter or during extended drought. In the spring, fall, and

following precipitation events when roots were physiologically active, melanized fungal structures decreased and a

corresponding increase in unique vacuolated hyaline hyphae were observed. Hyaline hyphae were more frequently

associated with metabolically active roots and were considered active stages of DS fungi. Hyaline hyphae form an

extensive inter- and intracellular network within the cortex

and sieve elements. In the cortex, hyphae were larger, 2 to

5 μm diameter, and had distinctly visible walls. Within the

sieve elements, they were smaller in diameter, 1 to 2 μm, and

their walls were less visible. Staining with sudan IV positively stained lipids in fungal vacuoles further enhancing

the visibility of internal colonization of DS fungi.

Lipid accumulation in fungal vacuoles was highly variable

and was also influenced by physiological activity of the roots.

Lipids began to accumulate in spherical fungal vacuoles in

hyphae growing in the cortex and in the vascular cylinder in

early spring before any growth response was observed and

continued until new leaves were established, at which time

lipids were not observed in fungal vacuoles. Lipid accumulation was again observed in fungal vacuoles in response to

intense, short duration precipitation events that increased

soil moisture in late summer then they decreased as soil

moisture decreased. In late fall, as mean temperatures

dropped, fungal vacuoles again accumulated substantial

lipids in the cortex. The vacuoles were elongated and more

abundant than the smaller, more spherical vacuoles observed in the spring.

Discussion _____________________

Dark septate fungal endophytes are not only the dominant colonizers of native plant roots in arid southwestern

rangelands (Barrow and others 1997), but they are wide

spread in other stressed ecosystems (Jumpponen and Trappe

1998). The staining of colonized roots with sudan IV and

analysis with DIC (Barrow and Aaltonen 2001) revealed

extensive internal colonization by hyaline hyphae that are

not evident using conventional fungus staining methods.

Dark septate fungi are highly polymorphic and produce

hyaline internal structures from external pigmented septate hyphae (Barrow and Aaltonen 2001; Haselwandter and

Read 1982; Newsham 1999). They form unique nondestructive internal interfaces with cortical cells and sieve elements. Their cumulation of substantial quantities of lipids

in response to physiological activity suggests that they have

a significant ecological role in the transport and management of carbon.

The small diameter hyaline hyphae that nondestructively

colonize the sieve elements are virtually indistinguishable

with DIC microscopy because they lack chitin and melanin

and are very thin walled. These characteristics would increase their permeability and facilitate resource exchange

with the host (Barrow and Aaltonen 2001; Cousin 1996;

Money and others 1998). The accumulation of lipids in

fungal vacuoles within the sieve elements (carbon transport

cells) suggests that the fungus is accessing host photosynthate and converting it to fungal lipids. The amount of lipids

within hyaline hyphae in both the vascular cylinder and the

cortex suggests that they are being transported by the

fungus, but the direction of carbon transport is not clear.

Both pathogenic and symbiotic fungi access photosynthetic

carbon from their hosts. DS fungi accumulate substantial

quantities of lipids without any deleterious effects on the

host suggesting that they manage carbon for the benefit of

the host.

Mycorrhizal fungi not only enhance nutrient and water

uptake in exchange for carbon, but they also contribute other

significant ecological factors that enhance the stability and

survival of native plant communities. They increase total

chlorophyll and carotenoid content of host plants, accelerate

net photosynthesis, increase total carbohydrate accumulation in the roots, and carbon flow into the soil contents

(Graves and others 1997). Soil organic carbon and nitrogen

pools were found to be 13 percent greater under tall fescue

pastures with high fungal endophyte colonization compared

with soil pools under low colonized pastures (Franzluebbers

and others 1999). Plants likewise exude substantial quantities of carbon as simple sugars, organic acids, and polysaccharides in the rhizosphere (Isobe and Tsuboki 1998) into

the soil that favorably modifies the microenvironment of the

rhizosphere, improving soil properties and enhancing plant

stability (Grayston and others 1997; Perry and others 1992).

Mucigels or polysaccharides have high water binding capacity (Chenu and Roberson 1996), maintain hydraulic continuity between the root and soil (Read and others 1999), and

enhance nutrient diffusion and uptake in dry soils

(Sutherland 1998). Organic acids change pH and enhance

mineralization and nutrient uptake (Jones 1998). Soil

polysaccharides are polymers of simple sugars, which are

released by hydrolysis and provide an energy source for soil

microflora involved in mineralization (Bianciotto and others

1996). Soil carbon enhances soil aggregation and stability,

water-holding capacity, and serves as an energy reserve for

plants and microbes.

It is proposed that DS fungi stimulate photosynthesis,

convert host photosynthate to lipids, transport it to the soil
USDA Forest Service Proceedings RMRS-P-21. 2001 293

Carbon Transport by Symbiotic Fungi in Fourwing Saltbush, Atriplex canescens (Pursh) Nutt. Barrow

where it insulates plant roots allowing them to survive and

function in harsh dry soil. The dynamic and variable response of lipid accumulation by DS fungi as it was influenced

by physiological activity of the host suggested the potential

of bidirectional transport of carbon between the host and the

soil. In the spring, before any new growth was evident and

when photosynthetic activity was low, substantial lipid

transport and accumulation was observed in hyphae in the

cortical cells and in the sieve elements. It is suggested that

the fungi were accessing carbon from soil reserves and

supplying the plant energy rich carbon for the synthesis of

new leaves, similar to the mechanism used by orchid mycorrhizal fungi, which degrade complex external carbohydrates

and supply the host with simple sugars for the production of

roots and shoots (Peterson and others 1998). After new

leaves were established and the host was presumed to be

photosynthetically active, lipid accumulation ceased. A pathogenic association would suggest that the fungi would extract

more carbon from the host when it was photosynthetically

active. It is suggested that DS fungi receive carbon from the

host to meet its physiological and growth requirements and

transport substantial quantities to the soil to recharge soil

supplies essential for water retention, mineralization, and

nutrient uptake. During periods of stress, they may reverse

the flow of carbon to supply the host sufficient energy rich

carbon for growth and survival.

The widespread colonization of native grasses and shrubs

by DS fungi in arid rangelands, their nondestructive interface with sieve elements, and accumulation of substantial

quantities of lipids during periods of peak physiological

activity in the host suggest that these fungi manage and

recycle carbon for the survival and stability of plant communities. Future studies must focus on the direction of carbon

flow, the nature of carbon profiles that are established in the

soil, and how they relate to ecosystem stability.

References _____________________

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Barrow, J. R.; Havstad, K. M.; McCaslin, B. D. 1997. Fungal root

endophytes in fourwing saltbush, Atriplex canescens, on arid

rangelands of southwestern U.S.A. Arid Soil Research Rehabilitation. 11: 177–185.

Barrow, J. R.; Aaltonen, R. E. 2001. A method of evaluating internal

colonization of Atriplex canescens (Pursh) Nutt. roots by dark

septate fungi and how they are influenced by physiological

activity. Mycorrhiza. [In press].

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In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Lee Walls is a Graduate Student, Department of Natural Resource Sciences, Washington State University, Pullman, WA 99164. Benjamin A.

Zamora is an Associate Professor and Range Scientist, Department of Natural

Resource Sciences, Washington State University, Pullman, WA 99164.

Nitrogen-Fixing Nodule Characterization

and Morphology of Four Species in the

Northern Intermountain Region

Lee Walls

Benjamin A. Zamora

Abstract—Purshia tridentata (antelope bitterbrush), Ceanothus

velutinus (snowbrush), Ceanothus sanguenius (redstem ceanothus),

and Shepherdia canadensis (buffaloberry) are native shrubs of the

Northern Intermountain Region that are generally characterized as

nitrogen-fixing species. These species occupy a range of habitats

from steppe to alpine environments. Nodulation of these species is

initiated through root infection by Frankia species and the resulting

nodules are described as coralloid. Nodulation is not necessarily

confirmation that nitrogen-fixation is taking place in the nodular

and root tissue of the shrub. Nodule formation, abundance, and

functionality on individual plants is strongly influenced by soil

moisture, soil nutrient balance, and age and health of the individual

shrub, thus the character of nitrogen-fixation as an ecological

process across a shrub population, and through time, may be

tremendously varied. We determined the degree of nodulation and

the nodule morphological characteristics on plants between stands

and sites to be consistent.

Introduction ____________________

Non-legume nitrogen-fixing shrubs are frequently among

the first colonizers on disturbed forest and range sites

especially when nitrogen availability is one of the principal

limiting factors. Non-leguminous shrubs and trees that fix

atmospheric nitrogen for plant use are known as actinorhizal

plants and the roots of these plants form a symbiotic relationship with an actinomycete in the genus Frankia.

Actinorhizal plants are found almost everywhere in the

world and most species, as far as is presently known, are

found in temperate climate regimes.

The potential to incorporate actinorhizal plants in the

design of vegetative covers for severely disturbed areas is

great and often a significant means of stimulating and

stabilizing nutrient cycling on these sites. In this paper we

have documented the nitrogen-fixing nodular structures on

each of four native woody shrub species found in the Northern Intermountain Region. This study is part of a large

research effort examining soil nutrient regimes that will

promote native vegetative development on severely disturbed sites. Initially, we assumed that each species has

distinct nodule morphology. Our study focused on characterization of nodule morphology but included nodule occurrence within a stand, nodule placement on individual roots

and root types, and the mode of nodule attachment to roots.

The character of nodules that occur on these wild plants will

be used as a means for comparison to nodule development on

experimentally grown plants being researched for reclamation of severely disturbed landscapes.

Nodule Form and Function in Wild Nitrogen-Fixing

Plants—Knowledge of Northern Intermountain Region

actinorhizal plants in the wild is limited. The majority of

research has been made on agricultural and horticultural

nitrogen fixation and nitrogen fixation under controlled

conditions. Relatively few research efforts to this point have

addressed native nitrogen-fixing plants in the wild and the

role they can play in reclamation vegetation cover in severely disturbed landscapes in the Northern Intermountain

Region. Genera receiving the most research are Alnus,

Ceanothus, and Purshia in that order. In the United States

there are over a 100 actinorhizal native species and several

naturalized species considered to be noxious weeds (Paschke

1997). The genus with the greatest number of actinorhizal

species is Ceanothus. This genus has more than 30

actinorhizal species. Ceanothus and Purshia are the most

prevalent actinorhizal shrub genera in the Northern Intermountain Region. In the Northern Intermountain Region of

North America there are several nitrogen-fixing woody

species (table 1) that are important as wildlife cover, livestock and wildlife browse, and considered pioneers in ecological succession.

The site of nitrogen fixation is in nodules on plant roots

(fig. 1). Morphologically, nodules in actinorhizal species are

modified lateral roots. The nodulation originates in the

pericycle of the root (Strand and Laetsch 1977; Berry and

Sunell 1990). Frankia infections are known to initially take

place by intracellular penetration in which the bacteria

enters a deformed host root hair and by an intercellular host

cell penetration that is capable of infecting multiple sites in

mature root cortical tissues. The type(s) of infection depends

on the host plant species (Berry and Sunell 1990). Vascular

tissue is central in the nodule and the bacterial organisms

are found in the cells of the nodule cortex. This is different

from the structure of legume nodules that are more tumorlike in which vascular tissue surrounds the nitrogen-fixing

organism (Baker and Schwintzer 1990). The stele in nodules

is not invaded by the Frankia bacteria and there are no root

hairs, root cap (Nelson and Schuttler 1984), or root epidermis (Strand and Laetsch 1977).
296 USDA Forest Service Proceedings RMRS-P-21. 2001

Walls and Zamora Nitrogen-Fixing Nodule Characterization and Morphology of Four Species in the Northern Intermountain Region

Table 1—Pacific Northwest native nitrogen-fixing shrubs and trees of forests and rangelands.

Environments

Moist Dry

Family Genus Species forest forest Subalpine Steppe

Elaeagnaceae Shepherdia canadensis +

argentia +

Elaeagnus commutata +

Myricaceae Myrica californica +

gale +

Betulaceae Alnus rubra +

incana +

rhombifolia +

sitchensis +

Rhamnaceae Ceanothus velutinus +++

sanguineus + +

cuneatus +

integerrimus +

prostratus +

Rosaceae Cercocarpus ledifolius + +

montanus + +

Dryas drummondii +

integrifolia +

+

Purshia tridentata + +

Symbiotic

Vesicle—Site of

N2 Fixation

Nodule

Lobe

Nitrogenase

Nodule Root

Nitrogen as

Amino Acids&

Amides

NH4

+

NH4

+ NH4

+

NH4

+

NH4

+

O2

Pathway

Nitrogen

Leakage into

Rhizosphere?

Multilaminate

Vesicle Monolayer

Lipid Envelope—Provides

O2 Diffusion Resistance

Xylem

N2

Figure 1—Generalized process of nitrogen-fixation (adapted from Huss-Danell 1990; Silvester

and others 1990; Smith and others 1999).

The enzymatic reduction of atmospheric nitrogen is relatively slow and very expensive in terms of ATP provided by

the host plant (Huss-Danell 1990; Sprent 1993). Because

large amounts of ATP energy are consumed for metabolic

activities and nitrogen fixation, the nodules require increased amounts of oxygen energy derived from plant respiration. At the same time the need for oxygen is increased,

nitrogenase has to be protected from oxygen exposure because the enzyme is lethally sensitive to it (fig. 1). The host

cell wall and plasmalemma surround the bacteria and are

thought to afford it the needed protection (Silvester and

others 1990).

Frankia induced nodules have been described in almost

all actinorhizal species as coralloid clusters and consist of

multiple dichotomously branching lobes (Krebill and Muir

1974; Wood and others 1989). Their colors range from light

tan to dark brown (Krebill and Muir 1974) and almost

whitish (Nelson 1983).

Various authors have determined that Frankia nodules

are perennial (Strand and Laetsch 1977; Nelson and Schuttler

1984). A nodule cluster may arise from a single infection site

and may be effective for several years in the field (Schwintzer

and Tjepkema 1996). The nodules, as does the whole plant in

temperate regions, become dormant in the winter (HussDanell 1990). Kummerow and others (1978) determined the

age of some Ceanothus species nodules to be 6 to 8 years old.

Nelson (1983) observed Cowania stansburiananodules to be

on roots that were distinctly larger than roots of a comparable age. He postulated that this root enlargement was

perhaps hormonally mediated and contributed to longevity

of nodules as well as more secure nodule attachment and

provided for the larger volume of needed vascular

translocation.

Atmospheric nitrogen is reduced by a bacterial nitrogenase enzyme system provided by the Frankia species. Nitrogenase catalyzes the dinitrogen reduction reaction to form

the ammonium ion (Huss-Danell 1990). Ammonium is a

form of nitrogen able to be used by plants (Sprent and Sprent

1990) and can give them a survival advantage in nitrogen

limited environments (Wollum and Youngberg 1969; Postgate

1982; Righetti and others 1986; Sprent 1993; Walker 1993;

Kohls and others 1994; Paschke 1997).
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Nitrogen-Fixing Nodule Characterization and Morphology of Four Species in the Northern Intermountain Region Walls and Zamora

Only the distal portion of nodules (about 10 to 20 percent of

live weight) is known to be fixing nitrogen (Kummerow and

others1978). The tips of nodules are much lighter than the rest

of the nodule. The number of nodules clusters on each plant is

inversely correlated to the mass of the nodules (Sangina and

others 1996). There appear to be large differences in the

numbers of nodules between Cowaniaand Purshiaspecies and

the nodule clusters are often larger on field plants that have

fewer numbers of nodules (Nelson 1983).

Nodulation and nodule activity generally thrive when the

whole plant thrives and are affected by pH, temperature,

and available moisture. Optimal pH range is 6.5 to 8.0 and

below 5 nodules become inactive (Alexander 1977). Burggraaf

and Shipton (1982) found some Frankia isolates to grow well

on media at pH 6.5 to 7.0 but can extend their range from 4.6

to 8.0. Generally, actinomycetes temperature range for optimal growth is 29 to 37 °C. There is little growth below 5 °C

and none at 39 °C (Alexander 1977). When soil temperature

at 20 cm is increased above 10 °C (Dalton and Zobel 1977)

nodule growth and activity begins. Under strongly aerobic

conditions, Frankia require temperatures of around 25 to

30 °C (Stowers 1987). Youngberg and Wollum (1976) feel the

optimal temperature for nodule activity is 23 °C.

Nitrogenase is severely depressed under even slight soil/

water deficit (Abdel Wahab and Abd-Alla 1995). Righetti

and others (1986) found evidence that nodules slough off in

dry years. In excessive water they fail to thrive because

when O2 is lacking they cannot metabolize (Alexander 1977).

Righetti and Munns (1981) thought nitrogen additions

inhibited nodulation and nodule activity. However, nitrogen

levels in the soil were not thought to be the reason for lack

of nodules or nodule nitrogen fixation activity (Righetti and

others 1986). When nitrogen is supplied to plants the roots

form more callus than plant roots grown in nitrogen deficient soil. Callus is incapable of fixing nitrogen.

Nodulation does not necessarily mean nitrogen fixation is

taking place and some nodules exist but never fix nitrogen

(Kohls and others 1994). Nitrogenase activity is one means

by which researchers have been able to measure nitrogen

fixation. Several methods of measuring nitrogenase activity

have been available for the past 40 years and of these

methods, acetylene reduction assay has been determined to

be the most sensitive and the least expensive (Sprent 1979).

Estimates of nitrogen addition by Ceanothus species systems are more a function of the Frankia species than the host

species (Nelson and Lopez 1989). Nitrogen fixation rates are

also thought to vary with plant species and Frankia combination, plant and nodule age, growth conditions in the field,

time of day, season of the year, method of measurement, and

how the rates are expressed (Huss-Danell 1990).

Seasonal patterns of nodule lobe growth and nitrogenase

activity have been studied to some extent and are found to

vary throughout the growing season. In central Oregon,

nodule growth and activity in Purshia tridentata begins

mid-May at the time the soil temperature at 20 cm below the

surface rises above 10 °C. The greatest nodule activity

appears to be in late June, and in July. In late July and

August, activity declines with higher air temperatures and

increased water stress (Dalton and Zobel 1977). The nitrogenase enzyme system is greatly affected by water stress and

depletion of carbohydrates derived from photosynthesis is

often effected by stomatal closure (Dalton and Zobel 1977).

Dalton and Zobel (1977) also found diurnal and seasonal

diurnal patterns in nitrogen-fixation activity. Rates of acetylene reduction were low at predawn and late in the afternoon. Activity was greatest in the mid day. The declines in

nodule activity were greater from June to August than were

the mid day nitrogenase reduction rates.

The Role of Nitrogen-Fixing Woody Plants in Revegetation—Purshia tridentata is a dominant in several distinct climax forest and steppe vegetation types of the Northern Intermountain Region. Because of its prevalence in

some areas, it may also occur as an early seral species on

xeric soils. Purshia tridentata will commonly colonize recently burned Pseudotsuga menziesii sites and dominate the

shrub layer until shaded out by other shrubs or development

of an overstory tree layer. Purshia species can pioneer on

semiarid foothills, plains, and mountain slopes and nodulation within the first 20 to 30 cm of root depth might be

important for vegetation establishment in nitrogen deficient

pioneer situations (Righetti and others 1986). Field observations show moisture is the limiting factor in nodule formation (Kummerow and others 1978). When nitrogen in the

system is limiting and other factors are plentiful, nitrogenfixing symbioses can have a significant role. Once nitrogen

is no longer limiting, nitrogen fixers are not as competitive

and other species take over in succession (Sprent 1993).

Sprent (1993) postulated removal of nitrogen limitations

could encourage more rapid cycling of all nutrients and lead

to possible losses due to leaching and addition of nitrates to

groundwater (Sprent 1993).

Both Ceanothus velutinus and Ceanothus sanguineus are

most prevalent during the early vegetation stages of disturbed forest sites where the overstory layer has been

removed and the site subjected to fire. Ceanothus species are

also very often present following stand-replacing wildfire

events. Because of surface and soil depletion by fire and

other soil disturbances, these sites are generally considered

deficient if not devoid of available soil nitrogen. Youngberg

and Wollum (1976) estimated that Ceanothus velutinus

brings nitrogen concentrations up to pre-burn levels in just

7 years.

Shepherdia canadensis is most prevalent in more advanced successional stages of disturbed forest vegetation

and is present, but not dominant, in old-growth forests. In

early succession, Shepherdia will maintain itself as part of

the seral vegetation.

Nitrogen-fixing plants are able to survive in environments

unfavorable to other plants and, therefore, build up organic

matter. Woody nitrogen fixers, in addition to adding to

nitrogen accumulation in the soil in the form of dead leaf and

root tissue, can affect other species’ successful colonization

by providing shade, moist microsites, seed capture, and soil

stabilization. In fact, nitrogen fixation may not be the most

important contribution. Actinorhizal species such as Alnus

rubra when planted with Pseudotsuga menziesii tend to

suppress fungal root diseases and increase wood production

in the conifer (Dawson 1990). Nitrogen fixers can sustain

themselves in otherwise limiting environments and by the

mere fact of their presence, pave the way for later successional species (Walker 1993). Pioneer succession plants add

to soil organic matter. Ceanothus velutinus is one of the

species that increases soil organic matter. Organic matter is
298 USDA Forest Service Proceedings RMRS-P-21. 2001

Walls and Zamora Nitrogen-Fixing Nodule Characterization and Morphology of Four Species in the Northern Intermountain Region

the primary storage medium for soil N and the relatively

decay resistant nature of humidified organic matter means

that chemically bound organic nitrogen will be released

fairly slowly (Hibbs and Cromack 1990). Soil pH can be

reduced, which will minimize nitrogen and ammonia losses

due to volatization (Alexander 1977) but can increase the

loss of cations by encouraging their release from soil and

subsequent loss by leaching (Paschke and others 1989).

The role of nitrogen fixers in revegetation has only been

postulated based on inference that nitrogen fixers put nitrogen back into their environments (Munshower 1993). Nitrogen-fixing plants can also become a trapping mechanism for

nitrogen and in turn, release it slowly into its soil environment. Dawson (1993) estimated tropical systems to be some

of the most important nitrogen-fixing systems on the earth

but estimates of their contribution to global nitrogen fixation may be underestimated because accurate data from

these areas are lacking. Burns and Hardy (1975) estimate

4,100 x 106 ha in forests and woodlands to be responsible for

fixing 10 kg nitrogen per hectare per year. This amounts to

28 percent of terrestrial ecosystems’ contribution of nitrogen

fixed every year.

Others working with actinorhizal nitrogen fixers have

obtained specific results that vary from 0.057 kg N ha–1

yr–1 in Purshia tridentata (Dalton and Zobel 1977), 80 kg

N ha–1 yr–1 for Ceanothus velutinus (Cromack and others

1979), 24–50 kg N ha–1 yr–1 in Ceanothus sanguineus

(Binkley and Husted 1983), 42–100 kg N ha–1 yr–1 for

Ceanothus in the Pacific Northwest (Binkley and others

1982), 101 kg N ha–1 yr–1 (McNabb and Cromack 1983), and

50–200 kg N ha–1 yr–1 for Alnus rubra (Hart and others

1997).

Most woody tree and shrub actinorhizal plants are shade

intolerant early colonizers of disturbed sites. Ceanothus

velutinus is considered to compete negatively with

Pseudotsuga menziesii in regeneration of severely disturbed

sites (Dawson 1990). On the other hand, Binkley and others

(1982) argue that Ceanothus velutinus competes for water,

light, and nutrients early on in the stand regeneration but

over time, nitrogen accretion is enough to compensate for

nitrogen losses generated by the disturbance. They feel the

species is critical in regeneration of secondary successional

sites.

Actinorhizal plants can also benefit from associations

with other plant species. In Alnus rubra stands, for instance,

associated species such as Thuja plicata offer wind protection and controlled spacing, resulting in increased tree

diameter and straighter stems (Dawson 1990).

Materials and Methods

The incidence and morphology of nitrogen-fixing nodules

were examined on the shrubs Purshia tridentata, Ceanothus

velutinus, Ceanothus sanguineus, and Shepherdia canadensis. These species are native to the Northern Intermountain Region and are being studied for their utility in reclamation vegetation covers.

Sample Populations—Three areas in Washington and

Idaho were chosen for collection of plant materials for all

four species.

Two populations of Purshia tridentata were sampled on

the Spokane Indian Reservation, Stevens County, eastcentral Washington. Both sites are near the abandoned

uranium Midnite Mine for which native vegetation covers

are being studied. The soil of both sites is sandy gravel

glacial till and both belong to the Pinus ponderosa/Purshia

tridentata habitat type.

Three populations of Shepherdia canadensis plants were

sampled. Two of the sites are on the Spokane Indian Reservation. Both sites had been logged and prescribed burned

within the last 5 years and represent the Pseudotsuga

menziesii/Calamagrostis rubescens and the Pseudotsuga

menziesii/Symphoricarpos albus habitat types. The third

population is from a gravely soil, Pseudotsuga menziesii/

Symphoricarpos albus habitat type that was also recently

logged and burned. This site is south of Thrapp Mountain,

Twisp Ranger District, Wenatchee National Forest,

Okanogan County in north-central Washington.

Ceanothus velutinus was taken from the same Okanogan

site. A second population of Ceanothus velutinuswas sampled

from disturbed sites in a Tsuga heterophylla/Clintonia uniflora habitat type of the St. Joe National Forest, Potlatch

Ranger District, Idaho. All soils of these sites were a gravely

sand.

Ceanothus sanguineus was located the same area as the

first Shepherdia and second Shepherdia sites.

Sample Collection and Analysis—Fifteen cubic decimeters soil (65 cm diameter by 45 cm deep) with root

material were carefully removed from around the root crown

of each shrub. On every plant, all nodule distances from the

crown were noted. The number of nodules and their root

attachments were recorded. Crown height and dry weights,

and root length and dry weights were determined. Nodules

were carefully examined, photographed, and dry weights

taken. Averages of data from plants in each species were

computed for comparison between species.

Results and Discussion

Species Characteristics in the Northern Intermountain Region—Purshia tridentata in the Northern Intermountain Region is often a species with winter persistent

leaves and found in low elevations with coarse textured,

well-drained soils. It is considered a late successional species but can be an early colonizer on disturbed sites of more

moist habitat types. It is found on warm, dry sites in steppe

and forest zones. Purshia quickly develops a large, single,

deep taproot that appears to be an adaptation to survive in

water stressed habitats.

Ceanothus velutinus is an early seral evergreen species

found on Pseudotsuga menziesii to warm Abies lasiocarpa

habitat types. This species is best adapted to dry forest

conditions and grows on hillsides and is commonly found on

coarse textured soils. This forest shrub is not shade tolerant

and is limited in its successional role to early states of

vegetation development following fire and other kinds of

severe soil disturbances on cold and drought-prone sites.

This species is considered to have a deep taproot; however,

in our samples, none of the plants formed a distinct taproot.

The upper portion of the root beneath the caudex was a
USDA Forest Service Proceedings RMRS-P-21. 2001 299

Nitrogen-Fixing Nodule Characterization and Morphology of Four Species in the Northern Intermountain Region Walls and Zamora

single large diameter root that divided within a depth of 15

to 20 cm into small diameter, lateral, spreading roots.

Ceanothus sanguineus in the Northern Intermountain

Region is a deciduous forest shrub in the Pseudotsuga

menziesiito warm Abies lasiocarpa sites. It is a seral species

with low-moderate shade tolerance, grows on dry rocky

hillsides, and is fire adapted. The caudex develops into a

large structure that resembles the start of a taproot but no

distinct taproot was evident in any of the plants we sampled.

Primary branching produces fairly large lateral branches.

These lateral branches became a diffuse root system within

a short distance from the plant. It is more drought and cold

tolerant than Ceanothus velutinus and overlaps Ceanothus

velutinus in range and habitat characteristics (Hibbs and

Cromack 1990).

Shepherdia canadensis is a deciduous forest shrub found

on moist, cool sites with fine to sandy, gravely, rocky soils. It

is found on Pseudotsuga menziesiito warm Abies lasiocarpa

sites. It is shade and fire tolerant. This species has no

distinct taproot and branching of the main lateral roots is

evident immediately below the crown.

Species Nodule Characteristics—In our Purshiastudy

areas, only 50 percent of the Purshia plants examined were

nodulated. The nodules were predominantly small masses of

8 mm in diameter with an average weight of.0.081 grams

(table 2). Single lobed nodule development was scarce and

the nodules were usually found on fine lateral roots at least

15 cm but no deeper than 25 cm below the crown of the plant.

No nodules were observed directly attached to the primary

root. The nodules were irregularly lobed globular clusters

and were very fragile, easily breaking apart from their

attachments to one another and associated roots to which

they were attached (fig. 2). There was a strong tendency for

the clusters to form a spherical shape.

Ceanothus velutinus nodules were irregularly shaped

lobed masses. Seventy percent of the plants excavated had

nodules at one site and 60 percent at the other site had

nodules. The nodules were large (33 mm diameter and dry

weight of 1.191 g), and relatively sturdy. Most of the nodules

were found at an average depth of 20 cm below the crown and

attached directly to the main root. A distinguishing characteristic of these nodule clusters was the long lobe roots. The

average nodule lobe root length was 5 mm (fig. 3) compared

to 3.5 mm and less in the other species we examined.

Ceanothus sanguineus nodules were generally large and

irregularly shaped masses. In comparison to Purshia and

Shepherdia, the nodules were large in size, averaging 24 mm

diameter, and heaviest in dry weight. Nodules in this

Ceanothus species were the least fragile of the four plant

species examined. The nodule lobes were thick, short, and

firmly attached to one another (fig. 4). Most of these nodules

were found on fine roots within 5 to 30 cm of the caudex.

Shepherdia nodules, in contrast to Purshia, were 80 percent attached immediately below the root crown and nodule

masses varied substantially in size from small to large.

Clusters of nodules in this species were also attached to

young, fine roots. Shepherdia nodules had a tendency to

branch in one plane only and produce fan-shaped masses

(fig. 5) even when nodules’ growth were not restricted by

rocks in close proximity. This species often had numerous

strings of single lobed nodules along roots.

General Observations—There was a greater tendency

for larger nodule masses to form rather than single lobed

structures. With each species, we found that as the root

Table 2—Characteristics of plants and attached nodule clusters in field-collected samples.

Purshia Ceanothus Ceanothus Shepherdia

Character tridentata velutinus sanguineus canadensis

Plant and stem mean 111 209 125 187

dry weight (g) range 114–259 14–612 62–180 63–416

Plant age (yr) mean 7 11 5 6

range 2–5 7–18 3–8 3–9

Percentage of plants 50 65 100 100

with nodules

Sites of nodule 10% lateral off 100% primary root, 100% lateral root off 100% lateral root off

attachment secondary root, 85% some lateral primary root primary root

lateral off primary, 5%

tap root

Number of nodule mean 8 many 19 13

clusters in sample range 1–26 3 to many 4–59 3–37

Diameter of mean 8 33 24 19

clusters (mm) range 1–14 10–55 10–47 3–27

Tendency to 90% intermediate 100% very large 90% small clusters 20% intermediate, 80%

form clusters clusters form clusters form form small single lobed

nodules

Nodule dry weight (g) mean 0.081 1.191 0.142 0.096

range 0.012–0.218 0.212–2.547 0.017–0.644 0.01–0.0259
300 USDA Forest Service Proceedings RMRS-P-21. 2001

Walls and Zamora Nitrogen-Fixing Nodule Characterization and Morphology of Four Species in the Northern Intermountain Region

diameter increased, there was a greater prevalence of

senesced nodule masses. The most viable nodular masses

were strongly associated with younger and smaller roots.

Nodules were generally found within the first 10 to 30 cm

below the root crown of the plants examined. Nodules also

tended to be present on lateral roots off secondary roots.

Each of the actinorhizal species examined in this study

had nodules with physical features that were distinct for the

host plant. Distinguishing external morphological features

set them apart from one another based on size and form of

nodule mass, cluster weight, fragility of nodule tissue, and

nodule root characteristics.

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302 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Benjamin Zamora is Associate Professor, Natural Resource Sciences, and

Thomas Gnojek was a Graduate Research Assistant, Department of Forestry

and Range Management, Washington State University, Pullman, WA 99164.

Total Available Carbohydrates in

Serviceberry After Late Summer and

Fall Burning

Benjamin Zamora

Thomas Gnojek

Abstract—Total available carbohydrate (TAC) storage and depletion was measured in late summer and fall burned and unburned

serviceberry (Amelanchier alnifolia). The purpose of the study was

to assess the influence of late season prescribed fire on the vigor of

serviceberry, a key browse species on white-tailed deer (Odecoileus

virginianus ochrourus) winter range in northeastern Washington.

All plants displayed similar TAC cycles through the first growing

season following treatment. TAC levels in stems were highest prior

to bud activity and declined during the early stages of growth

(March, April, May). The low levels of stem TAC coincided with

periods of maximum stem growth. Roots had the highest TAC

concentrations prior to dormancy, then declined as stem elongation

progressed to mid-season. After maximum stem elongation, root

TAC levels increased significantly through the remaining growing

season. Late summer burned plants displayed immediate new

growth following treatment and advanced phenology during the

first growing season in contrast to fall burned and control plants.

The first year growth of fall burned shrubs was delayed until after

control plants had initiated stem elongation. Neither burn treatment had major impacts on carbohydrate storage nor vigor of shrub

growth.

Introduction ____________________

Serviceberry (Amelanchier alnifolia) is a preferred winter

browse for white-tailed deer on many habitat types

of northeastern Washington and adjacent Idaho. The shrub

is common in late stages of forest vegetation succession in

the Northern Intermountain Region but is most abundant in

the early stages of vegetation development following fire.

Serviceberry is a prolific resprouter following fire (Leege and

others 1971; Miller 1976). Most of the prescribed burning to

enhance deer winter habitat in northeastern Washington is

conducted during the fall season. The time of burn varies

according to fuel and weather conditions, but commonly

burns are conducted prior to onset of winter dormancy in

many of the browse species of the area. Concern was raised

about the potential influence of late summer and early fall

burning on browse recovery if browse species were burned

while still in active growth at the time of the burn. A key

physiological function in woody plants is the storage of

available carbohydrates produced by photosynthesis in excess of plant maintenance (Chapin and Shaver 1990; Coyne

and others 1995). This function provides an essential source

of energy for plant survival during dormancy and production

of plant tissue during early spring growth when carbohydrate utilization exceeds photosynthetic production. Interruption of the normal storage cycle of reserves in the later

stages of growth would potentially impact the survival,

vigor, and vitality of plants. Indication of such impact should

be apparent during the first growing season following

treatment.

The objective of this study was to determine the trends in

depletion and storage of total available carbohydrates within

various parts of serviceberry shrubs during the first growing

season following canopy removal by late summer and fall

burning.

Methods _______________________

Study Area

The study area is located on the Little Pend Orielle

Wildlife Recreation Area in Stevens County, northeastern

Washington. The area is controlled and managed by the

Washington State Game Department by permission of the

United States Fish and Wildlife Service of the Department

of the Interior who retains ownership. Location is 18.5 km

east-southeast of Colville, Washington. Annual precipitation averages 40 cm. Snow provided approximately 32 percent of this moisture. Snow can be expected by November

and commonly remains on the ground from December through

February. White-tailed deer (Odecoileus virginianus ochrourus) occupy the area from mid-November to mid-March.

Average daily winter temperatures during this time range

from 20 to 35 °F. Summers are warm, and sunny with

regularly occurring light rainfall throughout the summer.

The elevational range of the area is 730 to 775 m. Soil

characters are strongly influenced by glacial till composition

overlain by erosionally deposited fines. The Douglasfir/mallow ninebark (Pseudotsuga menziesii/Physocapus

malvaceus) plant association represents more than 70 percent of the area’s vegetation (Williams and others 1990).

Serviceberry averages less than 9 percent canopy cover

throughout the study area. While not the most abundant

browse species of the winter range, this species is designated

a key management species because of its low abundance and

high browse preference to white-tailed deer.
USDA Forest Service Proceedings RMRS-P-21. 2001 303

Total Available Carbohydrates in Serviceberry After Late Summer and Fall Burning Zamora and Gnojek

Field Methods

Thirty-six shrubs were selected for early August and midOctober burn treatments. Twenty-five additional shrubs

were selected as control plants. Early August represents a

physiologically active mature shrub having achieved maximum stem elongation and supporting maximum leaf area.

Mid-October represents a fully dormant, leafless mature

shrub condition. Pre-burn characteristics of the shrubs are

shown in table 1. The biomass of each shrub was calculated

using regression equations relating biomass to individual

stem diameter at ground level length, and total canopy

volume of the plant. Total canopy volume was calculated

using the formula for a cylinder where the maximum diameter and the average height of the canopy are used as

dimension variables.

Each shrub was burned individually in the treatments.

Additional fuel was inserted into the canopy of each shrub in

order to achieve a complete canopy removal burn. This fuel

consisted of twenty 2 cm x 2 cm x 120 cm 200 g mill strips or

8 kg of air dry straw.

The control shrubs served as the base for comparison to

plants in the burn treatments. Four stems of each control

plant were labeled with small metal tags for repeated observation to characterize phenology and growth. Length measurements in mm were made from bud scars at the base of

the current year twig to the tip of the true-terminal bud.

Laboratory Methods

Burned and control plants were excavated during the first

growing season following treatment. Sampling was conducted according to the specific phenological stages of late

winter dormancy, active growth, end of stem elongation, and

total leaf senescence. Subsamples of small roots (less than 7

mm in diameter), large roots (greater than 7 mm in diameter), root crowns, current year stems, and second year wood

were collected. Samples were placed in plastic bags, labeled,

immediately frozen on dry ice, then transported to the

laboratory and stored in a freezer until freeze-dried. The

freeze-dried samples were ground in a Wiley mill through a

2 mm screen and stored in airtight jars at 68 °F until

analyzed. Total available carbohydrates (TAC) will be the

preferred term used throughout this paper to identify the

nonstructural reserve component which can be readily

metabolized by the plant (Weinmann 1947; McConnel and

Garrison 1966). The TAC was extracted from the ground

plant samples using 0.2N sulfuric acid as described by Smith

and others (1964). This method hydrolyzes TAC to reducing

sugars that can be measured quantitatively by the ShafferSomogyi copper-iodometric titration method outlined by

Heizne and Murneek (1940). Data were subjected to analysis

of variance and Duncan’s new multiple range test within the

GLM procedure of the Statistical Analysis System, 1979

Edition (Helwig and Council 1979). Significant differences

between means are interpreted at the 0.05 level.

Results and Discussion __________

Phenological Development

Serviceberry plants typically remain dormant through

the end of February. By early March, plants begin to enter

the active bud stage. This progresses to nearly 100 percent

expression of the active bud stage by end of April. At this

time, a small percentage of the plants begin to enter the bud

burst stage and express anthesis. By mid-May, all plants

had entered the bud burst stage and show anthesis and the

beginning of stem elongation. The maximum rate of stem

elongation occurs from early-May to mid-June. Maximum

leaf area generally is achieved by mid-June and will persist

as a physiologically active leaf set until mid-July. After this

point in time, insect depredation, water and heat stress, and

fungal disease begin to cause varying degrees of leaf senescence. Maximum stem elongation is achieved by early August. Leaf senescence started in ernest at the end of August

and is complete by early October. Leaf fall of senesced leaves

may extend into mid-November.

The phenological development of the burn treatment

plants was similar in timing and pattern to that of the

control plants with some important exceptions. All plants

burned in late summer regenerated a significant amount of

new stem and leaf growth within 1 month of the treatment.

The new leaf sets appeared vigorous and physiologically

active later into October. Fall burned and control plants did

not initiate new fall growth. In the first growing season

following treatment, all late summer burn plants initiated

growth well in advance of the fall burned and control plants.

The late summer burned plants became bud active in late

February with stem growth initiating by mid-March and

Table 1—Average total available carbohydrates (TAC) percentages across phenological stages for five plant

parts of unburned control plants.

Phenological stage

Maximum Entering

stem winter

Plant part Bud active Anthesis elongation dormancy

Current year stem *** 11.7 a 8.9 b 8.5 c

Second year stem 9.2 d 8.1 e 8.1 e 8.3 e

Root crown 8.7 e 7.2 f 7.6 g 9.3 d

Large roots 9.5 d 9.4 d 9.3 d 9.9 e

Small roots 7.3 f 7.8 g 9.4 d 7.4 f

***Current year growth had not been initiated by this date.

Means followed by the same letter are not significantly different at the 5 percent level of probability.
304 USDA Forest Service Proceedings RMRS-P-21. 2001

Zamora and Gnojek Total Available Carbohydrates in Serviceberry After Late Summer and Fall Burning

rapid stem elongation by early-April. Anthesis did not occur

in plants of either burn treatments. Both fall burned and

control plants followed an identical phenological pattern.

TAC Levels

The TAC depletion and storage cycle in the control plants

is shown in table 1. Generally, all stems were at high TAC

levels at the beginning of the bud active stage. TAC levels in

current and second year wood peaked at the time of anthesis,

then began a sharp decline as stem elongation accelerated.

TAC levels of these plant parts stabilized by the end of the

stem elongation period. These peaks in stem TAC coincide

with declining levels of TAC in roots, root crowns, and older

stem portions suggesting that stored TAC in these plant

parts is being translocated to new growth sites in the canopy.

After anthesis, the TAC levels in roots and root crowns began

to progressively increase through the remaining growth

period. All below ground parts combined, had higher concentrations of TAC than the aerial portions of the plants after

midseason.

Current year growth of burned plants was the only canopy

portion available for comparison to the control plants. The

seasonal trends in depletion and storage of TAC plants of both

burn treatments were generally similar to the control plants

(table 2). A significant reduction in current year stem TAC of

all burned plants occurred after anthesis, leveling off at the

end of stem elongation period. No significant differences were

found in the TAC trends of all treatment plants. Small roots

of late summer burn shrubs exhibited a continual decline with

a significantly lower level of TAC by early October. Small

roots of late summer burned plants began the season at higher

TAC levels than plants in other treatments. Excavation of

these roots indicated that they were actively growing at the

time. Garrison (1971) stated that stored carbohydrates are

not affected by top removal in many shrubs because small

roots store the bulk of carbohydrates needed by the plant.

Large root TAC remained fairly constant for the control and

fall burned shrubs with a small upward trend after anthesis

and maximum stem elongation. The late summer burned

plants showed a statistically significant increase in TAC

levels between the end of stem elongation and mid-October

dormancy. Root crown TAC remained constant for all burned

shrubs throughout the season.

Coyne (1969) felt maximum carbohydrate reserves are not

attained until a plant completes its annual life cycle and that

maximum plant vigor depends upon the level of TAC storage.

Interruption of this cycle by burning in early August, prior

to completion of serviceberry’s growing cycle did not appear

to reduce serviceberry vigor during the first growing season

following treatment. Roots had the highest concentration of

TAC prior to dormancy. Therefore, as long as the root

component of the plant is not damaged by the late summer

fire, the crown portion is not requisite to the plant survival.

Coyne and others (1995) have suggested that fall growth

may tap stored reserves of the plant and stress the plant to

a point of low vigor, especially if repeated cropping of the new

growth is taking place. The fall growth of late summer

burned plants may potentially reduce TAC root levels to the

point of affecting the subsequent year’s canopy growth.

Continual crown removal has been shown in other studies

(George and McKell 1978) to affect root reserves and ultimately kill the plant. However, this was not evident in the

trends of TAC following treatment nor growth of plants in

this study.

References _____________________

Chapin, F. S.; Shaver, G. R. 1990. The ecology and economics of

storage in plants. Ann. Rev. Ecol. Syst. 21: 423–447.

Coyne, P. I. 1969. Seasonal trends in total available carbohydrates

with respect to phenological stage of development in eight desert

range species. Logan: Utah State University. Dissertation

Coyne, P. I.; Trlica, M. J.; Owensby, C. E. 1995. Carbon and nitrogen

dynamics in range plants. In: Bedunah, D. J.; Sosebee, R. E., eds.

Wildland plants: physiological ecology and developmental morphology. Denver, CO: Society of Range Management: 59–167.

Garrison, George A. 1971. Carbohydrates reserves and response to

use. In: Wildland shrubs—their biology and utilization: symposium proceedings; 1971 July; Logan, UT. Gen. Tech. Rep. INT-I.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Forest and Range Experiment Station: 271–278.

George, M. R.; McKell, C. M. 1978. Nonstructural carbohydrate

depletion in snowberry (Symphoricarpos oreophilus). J. Range

Manage. 31: 46–48.

Table 2—Average total available carbohydrates (TAC) percentages across phenological stages for four plant parts of late

summer and fall burned plants during the first growing season following treatment.

Phenological stage

Anthesis/ Maximum Entering

Burn stem elongation stem winter

Plant part treatment Bud active initiated elongation dormancy

Current year stem Late summer 12.3 a 10.2 b 8.1 c 7.4 c

Fall *** 10.7 b 8.3 c 8.2 c

Root crown Late summer 8.5 a 8.5 a 7.8 b 7.9 b

Fall 8.2 c 8.2 c 8.8 d 8.6 d

Large roots Late summer 7.9 a 7.8 a 7.1 b 9.5 c

Fall 8.4 d 7.6 a 8.3 d 9.0 e

Small roots Late summer 9.4 a 8.4 b 7.8 c 7.1 d

Fall 7.3 d 8.0 c 7.4 d 8.5 b

***Current year growth had not initiated in this treatment by this date.

Within each plant part category, means shown in the 2 treatment rows followed by the same letter are not significantly different at the

5 percent level of probability.
USDA Forest Service Proceedings RMRS-P-21. 2001 305

Total Available Carbohydrates in Serviceberry After Late Summer and Fall Burning Zamora and Gnojek

Heinze, P. H.; Murneek, A. E. 1940. Comparative acccuracy and

efficiency in determination of carbohydrates in plant material.

Mo. Agr. Exp. Sta. Res. Bull. 314.

Helwig, J. T.; Council, K. A., eds. 1979. Statistical analysis system:

user’s guide. Raleigh, NC: SAS Institute, Inc.

Leege, Thomas A.; Hickey, W. O. 1971. Sprouting of northern Idaho

shrubs after prescribed burning. J. Wildl. Manage. 35(3): 508–515.

McConnell, B. R.; Garrison, G. A. 1966. Seasonal variations of

available carbohydrates in bitter brush. J. Wildl. Manage. 30:

168–172.

Miller, Melanie. 1976. Shrub response to fire in a Douglas-fir/

western larch ecosystem. Missoula: University of Montana. Thesis.

Smith, D.; Paulsen, G. M.; Raguse, C. Q. 1964. Extraction of total

available carbohydrates from grass and legume tissue. Plant

Physical. 39: 960–962.

Weinmann, H. 1947. Determination of total available carbohydrates in plants. Plant Physiol. 22: 279–280.

Williams, C. K.; Lilybridge, T. R.; Smith, B. G. 1990. Forested plant

associations of the Colville National Forest. Field Guide. Colville,

WA: U.S. Department of Agriculture, Forest Service, Colville

National Forest.
306 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Ronald E. Sosebee is Professor, Department of Range, Wildlife, and

Fisheries Management, Texas Tech University, Lubbock, Texas 79409.

Long-Shoot/Short-Shoot Phenomenon

in Woody Plants

Ronald E. Sosebee

Abstract—Shoot growth in shrubs is often overlooked as an important component of phenological development in woody plants. However, shoot growth dictates the pattern of growth of deciduous trees

or shrubs, especially following defoliation or canopy damage. In

general, woody shoots are divided into short- and long-shoots.

Short-shoots, sometimes called “spurs,” are reproductive shoots (in

other words, spurs on an apple (Malus pumila) tree). The longshoots, sometimes called “watersprouts,” are vegetative shoots.

From a management perspective, herbicidal control of shrubs (in

other words, mesquite (Prosopis glandulosa)) with long-shoots is

highly ineffective. All of the energy synthesized by the plant is

translocated to the long-shoot and converted to structural materials; in other words, stem growth. Similarly, one could postulate that

browsing during the long-shoot stage would not significantly impair

shrub viability if the shrub was healthy and vigorous at the time of

browsing. Likewise, pruning shrubs during long-shoot growth (in a

lawn or garden) stimulates “wolf-like growth” of the shrub. In

contrast, herbicidal control of shrubs during the short-shoot stage

usually conveys a high degree of success. Likewise, pruning or

defoliation during the short-shoot stage significantly reduces fruit

production.

Long-Shoots/Short-Shoots _______

Shoot growth in woody plants is seldom considered in

management decisions relating to grazing, browsing, chemical control, mowing, and so forth. Likewise, it is seldom

considered an important component of phenological development in woody plants. Yet, the type of shoot growth,

especially following defoliation or crown damage, dictates

the growth pattern of a deciduous tree or shrub when they

initiate spring growth, fruit production, or resprouting.

This paper is not intended to present new scientific results

or as a literature review of research that has been conducted

on the subject. Rather, it is an opportunity to describe longand short-shoots and to present some management implications relating to long- and short-shoot growth patterns. For

a basic understanding of long- and short-shoots (fig. 1), the

reader is referred to Dahl and Hyder (1977) and Dahl (1995).

In general, shoot growth of woody plants is divided into

long- or short-shoots. In woody plants, long-shoots are vegetative shoots and short-shoots are reproductive shoots.

Long-shoots grow very rapidly (and remain vegetative) and

are called watersprouts in some species. They are major

energy sinks during rapid growth and internode expansion.

In contrast, short-shoots are sometimes called “spurs” (as in

apple (Malus pumila) trees) and are the shoots that bear

Figure 1—(A) Mesquite stem with predominantly

short-shoots (note almost total absence of internode elongation); (B) mesquite branch with a longshoot showing typical internode elongation. Source:

Dahl 1995.

short

shoots

long

shoots
USDA Forest Service Proceedings RMRS-P-21. 2001 307

Long-Shoot/Short-Shoot Phenomenon in Woody Plants Sosebee

fruit. Internodes are compressed and elongation is minimal.

Therefore, they are reproductive rather than vegetative

shoots. Since they are not rapidly expanding shoots, they are

not major energy sinks.

From a management perspective, it is important that one

recognize long- and short-shoot stages in plant development.

Any form of defoliation, damage, or injury to the shoots of

woody plants will stimulate long-shoot development. When

long-shoots are rapidly growing, they require a great deal of

energy that is synthesized by the plant to produce structural

materials in the long-shoots (in other words, stem growth).

Since these shoots are vegetative, shoot removal by grazing,

browsing, or even mechanical mowing during the long-shoot

stage would not be particularly detrimental to the tree or

shrub if the tree or shrub was healthy and vigorous at the

time of shoot damage or removal. Pruning shrubs in the

long-shoot stage, by whatever means (even in a lawn setting), often stimulates “wolf-like growth” of the tree or

shrub.

Foliar application of herbicides to resprouting woody

plants in the long-shoot stage usually results in ineffective

control. Since foliar-applied herbicides are generally translocated with the photosynthate (in other words, carbohydrate) stream, the herbicides would primarily be translocated to the shoots along with the carbohydrates for synthesis

of structural material and not to the perennating organs and

tissues that must be killed by the herbicide if chemical

control is to be effective.

On the other hand, defoliation or injury to the shoots of

woody plants in the short-shoot stage can be quite damaging

to a tree or shrub. Damage or removal of the short-shoots of

woody plants can significantly impair subsequent growth of

a tree or shrub. Any removal or damage to a shoot during the

short-shoot stage can significantly reduce fruit production

and development of new buds from which the subsequent

year’s growth and fruit production will originate.

Since the shoots are not primary sinks for photosynthates

during the short-shoot stage, the photosynthates (in other

words, carbohydrates) are translocated to the perennating

lateral buds (including basal buds) and storage tissues.

Therefore, chemical control of trees and shrubs is usually

quite successful when herbicides are foliar-applied during

the short-shoot stage (assuming that all other physiological

and environmental conditions are appropriate for control).

Interestingly enough, long- or short-shoot status of woody

plants is not necessarily related to chronological age of the

tree or shrub. For example, often one hears that control of

resprouts should not be planned for 5 to 7 years postresprouting, particularly in mesquite (Prosopis glandulosa).

However, our research indicated that dormant mesquite

shredded to ground level resprouted in the spring and

produced short-shoots during the first year of resprouting

(Beck and others 1975). Foliar-applied herbicidal control

was equally as effective on the first-year resprouts (shortshoots) as it was on 7- and 14-year old resprouts.

Without damage or defoliation to the shoots of woody

plants, trees and shrubs grow very methodically. The main

stem (or bole) of trees and shrubs is the first order long-shoot.

Stems branching off of the first order long-shoot (or lateral

stems) are second order long-shoots. Lateral stems branching off of second order long-shoots are third order longshoots, Usually as the order of long-shoots increase, fewer

and less vigorous long-shoots are produced. By the time the

trees and shrubs attain either fourth or fifth order longshoots, they produce no lateral long-shoots, only shortshoots. These short-shoots bear no long-shoots.

In summary, recognition of long- or short-shoot growth is

imperative in making woody plant management decisions.

How woody plants respond to grazing, browsing, mowing,

pruning, or herbicidal control depends upon whether they

are in the long- or short-shoot stage. As resource managers,

we should become cognizant of how trees and shrubs grow

and incorporate that knowledge into our management plans.

References _____________________

Beck, D.L.; Sosebee, R.E.; Herndon, E.B. 1975. Control of honey

mesquite by shredding and spraying. J. Range Manage. 28:

487–490.

Dahl, B.E. 1995. Developmental morphology of plants. In: Bedunah,

Donald J.; Sosebee, Ronald E., eds., Wildland Plants: Physiological Ecology and Developmental Morphology. Denver, CO: Society

for Range Management: 22–58.

Dahl, B.E.; Hyder, D.N. 1977. Developmental morphology and

management implications. In: Sosebee, Ronald E., ed., Rangeland Plant Physiology. Range Science Series No. 4. Denver, CO:

Society for Range Management: 257–290.
308 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Ricardo Mata-González was a Student, Universidad Autónoma Chapingo,

Unidad Regional Universitaria de Zonas Aridas, Bermejillo, Durango 56230,

México; currently he is a Research Associate, Texas Tech University, Department of Range, Wildlife, and Fisheries Management, P.O. Box 250, Sierra

Blanca, TX 79851. Rubén Meléndez-González was a Professor, Universidad

Autónoma Chapingo, Unidad Regional Universitaria de Zonas Aridas,

Bermejillo, Durango 56230, México. J. Jesús Martínez-Hernández was a

Professor, Colegio de Postgraduados, Campus San Luis Potosí, Salinas de

Hidalgo, San Luis Potosí 78600, México.

Aerial Biomass and Elemental Changes in

Atriplex canescens and A. acanthocarpa as

Affected by Salinity and Soil Water

Availability

Ricardo Mata-González

Rubén Meléndez-González

J. Jesús Martínez-Hernández

Abstract—Atriplex canescens and A. acanthocarpa from the

Chihuahuan Desert in México were subjected to different salinity

and irrigation treatments in a greenhouse study. Plants were grown

in pots containing soil and irrigated with NaCl solutions of 0, 50,

and 100 mM at 40 and 80 percent available soil water. Aerial

biomass of A. canescens declined as NaCl treatments increased. In

contrast, the aerial biomass of A. acanthocarpa was not negatively

affected by the salinity treatments, suggesting a high salt tolerance

of this species. Aerial biomass of A. acanthocarpa was more reduced

by the decrease in irrigation level than that of A. canescens. A.

acanthocarpa had a much higher accumulation of Na in leaf tissues

throughout the salinity gradient than A. canescens. Tissue concentration of K in both species was minimally affected by the salinity or

irrigation treatments. Leaf N concentration increased in both species as plants were subjected to higher salinity treatments. The

higher salt tolerance and higher Na absorption of A. acanthocarpa

favor the use of this plant in reclamation of saline areas, while the

low Na accumulation of A. canescens makes this species an attractive forage in saline rangelands.

Plants of the genus Atriplex are considered xero-halophytes for their ability to grow in dry and saline areas, which

allows them to succeed in many disturbed environments

(Osmond and others 1980). This characteristic makes Atriplex

spp. suitable plants for reclamation of highly disturbed

areas (Booth 1985). Some species of Atriplex are appreciated

as forage for livestock and wildlife since their nutritive value

is fairly high and their foliage is evergreen (Garza and

Fulbright 1988). The high biomass productivity of Atriplex

has motivated researchers to investigate the feasibility of

cultivating some species under seawater irrigation (O’Leary

and others 1985).

A. canescens is the most widely distributed Atriplex

species in North America and its ecophysiological characteristics, forage potential and genetic diversity have been

extensively studied (Glenn and others 1996; Cibils and

others 1998). A. acanthocarpa is a native shrub to North

America, has potential for revegetation in saline rangelands, and is considered a good forage for cattle and deer

(Garza and Fulbright 1988). However, this species has

received little attention from researchers and very little

is known about its salt tolerance and ecophysiological

characteristics.

It is important to study the salt tolerance characteristics

of halophytes because it could help to understand the potential utilization value of these plants and their ecological

adaptations. The present study was an attempt to evaluate

the effect of salinity and soil water availability on aerial

biomass and leaf concentration of Na, K, and N of A. canescens

and A. acanthocarpa. We hypothesized that increasing salinity levels has a negative effect on aerial biomass production of both species. The second hypothesis was that elemental changes are related to the characteristics of salt tolerance

of these species.

Materials and Methods ___________

This study was conducted in a greenhouse located in the

Unidad Regional Universitaria de Zonas Aridas, Universidad

Autónoma Chapingo, Bermejillo, Durango, México, in 1988.

Seeds of Atriplex canescens and A. acanthocarpa were collected from native populations near San Luis Potosí City and

Viesca, Coahuila, respectively. In April, seeds of both species

were soaked with distilled water, changing the water daily,

during 4 days. Subsequently, seeds were sown in germinating trays filled with a mixture of river sand (60 percent) and

soil (40 percent) and irrigated with water from local municipal supply. Seedlings emerged within 3 weeks, and 8 weeks

after sowing, one plant of each species was transplanted to

36 pots of approximately 3.5 L volume.

Pots contained a clay loam soil with low electrical conductivity (2 dS m–1) from Rancho El Cono, Salinas de Hidalgo,

San Luis Potosí. After plant establishment, plants of both

species were watered twice a week with solutions of 0, 50,

and 100 mM NaCl and maintained gravimetrically to either

40 or 80 percent available soil water. These treatments were

applied during 4 months. In October, the aerial part of the

plants were harvested, oven-dried and weighed to measure
USDA Forest Service Proceedings RMRS-P-21. 2001 309

Aerial Biomass and Elemental Changes in Atriplex canescens and A. acanthocarpa... Mata-González, Meléndez-González, and Martínez-Hernández

dry matter production. The leaves were separated and

ground to determine K and Na by flame emission with a

Varian AA-1275 atomic absorption spectrophotometer. Total Kjeldahl N was determined in leaves as outlined by

Bremner and Mulvaney (1982). The completely randomized

design was used in this experiment. The data were subjected

to analysis of variance, and mean separation tests at

P < 0.05 (protected Fisher’s LSD) were performed with a

Statistical Analysis System (SAS) computer program.

Results ________________________

Aerial biomass of A. canescens declined as NaCl concentration in the irrigation solution increased (fig. 1). A decrease of 37 percent in dry weight was observed in plants as

NaCl concentration increased from 0 to 100 mM. In contrast,

A. acanthocarpa did not show significant changes in aerial

biomass as a result of the salinity treatments (fig. 1). Aerial

biomass of A. acanthocarpa declined 20 percent in plants

irrigated at 40 percent available soil water compared to

plants irrigated at 80 percent available soil water (fig. 2).

On the other hand, the decrease in water availability did

not produce significant changes in the aerial biomass of

A. canescenes (fig. 2).

A low concentration of Na in leaves of both species was

observed in plants irrigated with 0 mM NaCl solutions and

increased in plants irrigated with 50 and 100 mM NaCl

solutions (fig. 3). A proportion of 1:2.4:2.7 reflected the

variation in leaf Na concentration of A. canescens irrigated

with solutions of 0, 50, and 100 mM NaCl, respectively. In

A. acanthocarpa the proportion of change was 1:2.1:2.3

(fig. 3). Although leaf Na concentration was similarly affected by salinity in both species, the Na concentration was

much higher in A. acanthocarpa than in A. canescens regardless of the salinity level (fig. 3). The concentration of K was

very similar in both species and it was not affected by the

salinity treatments (fig. 4). Irrigation treatments did not

exert a significant effect on leaf Na and K concentrations in

any species.

Salinity and irrigation treatments interacted to determine the variation of N concentration in leaves of A. canescens.

Plants irrigated at 40 percent available soil water had

higher N concentration than plants irrigated at 80 percent

available soil water when NaCl concentrations in the irrigation solution were 0 and 50 mM (fig. 5). However, plants

irrigated with solutions of 100 mM NaCl did not show

variations in N concentration due to changes in available

soil water. Regardless of the irrigation treatments, there

was a tendency to increase leaf N concentration as salinity

levels increased (fig. 5). Leaf N concentration in A. acanthocarpa was higher in plants irrigated with solutions of 100

mM NaCl than in plants irrigated with solutions of 0 and 50

mM NaCl (fig. 6). Irrigation treatments did not produce

significant changes in leaf N concentration of A. acanthocarpa.

Discussion _____________________

The decline observed in shoot growth of A canescens as

salinity levels increased has been previously observed (Glenn

and others 1994; Glenn and others 1996). The apparent high

salt tolerance of A. acanthocarpa has not been previously

a

a

a

b

c

a

A. canescens

A. acanthocarpa

NaCl Concentration (mM)

0 50 100

40

38

36

34

32

30

28

26

24

22

20

Aerial Biomass (g)

Figure 1—Aerial biomass (g) of Atriplex canescens and Atriplex acanthocarpa as affected by

NaCl concentration in the irrigation solution

(means with the same letter are not significantly

different at P > 0.05).

a

a

a

b

A. canescens A. acanthocarpa

40 percent Available Soil Water

80 percent Available Soil Water

45

40

35

30

25

20

15

10

5

0

Aerial Biomass (g)

Figure 2—Aerial biomass (g) of Atriplex canescens and Atriplex acanthocarpa as affected by

available soil water (means with the same letter are

not significantly different at P > 0.05).

reported but seems to be similar to that of Atriplex amnicola,

a halophyte that shows growth reduction only when the

salinity of the irrigation solution surpasses 100 mM (ElHaddad and O’Leary 1994). A. acanthocarpa seemed to be

more tolerant to salinity but less tolerant to drought than

A. canescens. In agreement with this, Wilkins and Klopateck

(1984) found that A. canescens had higher drought tolerance

than several other native shrubs in Arizona.
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Mata-González, Meléndez-González, and Martínez-Hernández Aerial Biomass and Elemental Changes in Atriplex canescens and A. acanthocarpa...

a

a a

a

b

b

A. canescens

A. acanthocarpa

NaCl Concentration (mM)

0 50 100

40

38

36

34

32

30

28

26

24

22

20

Leaf Na Concentration (percent)

a a

a

a

a

a

A. canescens

A. acanthocarpa

NaCl Concentration (mM)

0 50 100

8

7

6

5

4

3

2

1

0

Leaf K Concentration (percent)

40 percent Available Soil Water

80 percent Available Soil Water

NaCl Concentration (mM)

0 50 100

2

1.8

1.6

1.4

1.2

1

0.8

0.6

0.4

0.2

0

Leaf N Concentration (percent)

NaCl Concentration (mM)

0 50 100

1.4

1.2

1

0.8

0.6

0.4

0.2

0

Leaf N Concentration (percent)

a a

b

Figure 3—Leaf Na concentration ( percent) of Atriplex canescens and Atriplex acanthocarpa as affected by NaCl concentration in the irrigation solution

(means with the same letter are not significantly

different at P > 0.05).

Figure 4—Leaf K concentration ( percent) of Atriplex canescens and Atriplex acanthocarpa as

affected by NaCl concentration in the irrigation

solution (means with the same letter are not significantly different at P > 0.05).

Figure 5—Leaf N concentration ( percent) (± 1 SE)

of Atriplex canescens as affected by NaCl concentration in the irrigation solution and soil water

availability.

Figure 6—Leaf N concentration ( percent) of Atriplex

acanthocarpa as affected by NaCl concentration in

the irrigation solution (means with the same letter

are not significantly different at P > 0.05).

Na accumulation increased in A. canescensand A. acanthocarpaas plants faced increasing salinity levels. This response

has been previously reported in A. canescens (Glenn and

others 1996) and seems to be a typical response in halophytes.

Presumably, Na accumulation contributes to decrease leaf

osmotic potential in response to salinity increases in the root

medium (El-Haddad and O’Leary 1994). However, Na levels

in leaves of A. canescens were much lower than Na levels in

leaves of A. acanthocarpa irrespective of the salinity treatments. These results agree with those of Garza and Fulbright

(1988). Other studies have shown that under low salinity in

the root medium A. canescens tends to have lower Na levels

in leaves (Wallace and others 1973; Khalil and others 1986),

but higher Na levels in roots (Wallace and others 1973) than

other Atriplex species.
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Aerial Biomass and Elemental Changes in Atriplex canescens and A. acanthocarpa... Mata-González, Meléndez-González, and Martínez-Hernández

According to Glenn and others (1994) Na is the main

cation involved in the osmotic adjustment of A. canescens.

However, compared to other Atriplex species, A. canescens

seems to exclude Na from the leaves, as many crop plants do

to avoid Na damage to leaf tissues (Yeo and Flowers 1986).

The low Na accumulation in leaves of A. canescens is considered a reason for its high forage value (Wallace and others

1973), but this feature might be also associated with characteristics of low salt tolerance (Glenn and others 1994, 1996).

In agreement with this, results of this study showed that A.

canescens had lower salt tolerance and lower leaf Na levels

than A. acanthocarpa. The higher salt tolerance and Na

uptake of A. acanthocarpa make this species a viable candidate for reclamation of disturbed saline areas.

Leaf K concentration in both species remained very stable

and was not affected by salinity or irrigation treatments. K

is an essential nutrient for plants and its absorption, even

under salinity stress, must be maintained under acceptable

levels for plant survival (Grattan and Grieve 1992). K and

Na uptake by roots are competitive processes, but roots have

higher affinity for K than for Na absorption. This characteristic is particularly important in saline soils where Na is

much more available than K for plant uptake (Grattan and

Grieve 1992).

Leaf N concentration tended to increase in both species as

plants faced increasingly high salinity levels, although the

effect was more clearly expressed in A. canescens than in

A. acanthocarpa. This result could be partly a consequence

of the reduction in aerial biomass caused by salinity stress.

Pessarakli and others (1989) reported an increase of N

concentration and a dramatic decrease in dry matter yield in

salinized corn compared to control plants. Presumably,

salinity reduced dry matter yield more than N absorption

causing an increase in the concentration of N in leaves. A

similar effect was found in red kidney beans subjected to salt

and water stresses (Frota and Tucker 1978). In A. canescens

the low irrigation level also caused increases in N concentration compared to the high irrigation level under low and

intermediate salinity treatments. Apparently water stress

caused similar effects than salt stress reducing aerial biomass more than N absorption.

Conclusions____________________

Our results supported the hypothesis that increasing

salinity levels causes a decline in aerial biomass but only for

A. canescens. The salinity levels tested in this experiment

were not clearly deleterious for A. acanthocarpa, which

makes it a more salt tolerant species than A. canescens.

On the other hand, A. canescens was more tolerant to

drought than A. acanthocarpa. The higher salt tolerance of

A. acanthocarpa corresponded with a high capacity to accumulate Na ions in its leaves compared to A. canescens. This

supported our second hypothesis. N concentration increased

as salinity stress increased in both species, but more evidently in A. canescens, perhaps because N absorption was

less affected by salinity than plant growth.

References _____________________

Booth, T. D. 1985. The role of fourwing saltbush in mined reclamation: a viewpoint. Journal of Range Management. 38:562–565.

Bremner, J. M.; Mulvaney, C. S. 1982. Nitrogen-total. In: Page,

A. L., ed., Methods of soil analysis. Part 2. Chemical and microbiological properties. ASA-SSSA. Agronomy Monograph no. 9.

Madison, WI: 595–624.

Cibils, A. F.; Swift, D. M.; McArthur, E. D. 1998. Plant-herbivore

interactions in Atriplex: current state of knowledge. General

Technical Report RMRS-GTR-14. Ogden, UT: U.S. Department

of Agriculture, Forest Service.

El-Haddad, E. H. M.; O’Leary, J. W. 1994. Effect of salinity and K/

Na ratio of irrigation water on growth and solute content of

Atriplex amnicola and Sorghum bicolor. Irrigation Science. 14:

127–133.

Frota, J. N. E.; Tucker, T. C. 1978. Absorption rates of ammonium

and nitrate by red kidney beans under salt and water stress. Soil

Science Society of America Journal. 42:753–756.

Garza, A.; Fulbright, T. E. 1988. Comparative chemical composition

of armed saltbush and fourwing saltbush. Journal of Range

Management. 41:401–403.

Glenn, E. P.; Olsen, M.; Frye, R.; Moore, D.; Miyamoto, S. 1994. How

much sodium accumulation is necessary for salt tolerance in

subspecies of the halophyte Atriplex canescens? Plant, Cell and

Environment. 17:711–719.

Glenn, E. P.; Pfister, R; Brown, J. J; Thompson, T. L.; O’Leary, J.

1996. Na and K accumulation and salt tolerance of Atriplex

canescens (Chenopodiaceae) genotypes. American Journal of

Botany. 83:997–1005.

Grattan, S. R.; Grieve, C. M. 1992. Mineral element acquisition and

growth response of plants grown in saline environments. Agriculture, Ecosystems and Environment. 38:275–300.

Khalil, J. K.; Sawaya, W. N.; Hyder, S. Z. 1986. Nutrient composition of Atriplex leaves grown in Saudi Arabia. Journal of Range

Management. 39:104–107.

O’Leary, J. W.; Glenn, E. P.; Watson, M. C. 1985. Agricultural

production of halophytes irrigated with seawater. Plant and Soil.

89:311–321.

Osmond, C. B.; Bjorkman, O.; Anderson, D. J. 1980. Physiological

processes in plant ecology—toward a synthesis with Atriplex.

Berlin: Springer-Verlag. 463 p.

Pessarakli, M.; Huber, J. T.; Tucker, T. C. 1989. Dry matter yield,

nitrogen absorption, and water uptake by sweet corn under salt

stress. Journal of Plant Nutrition. 12:279–290.

Wallace, A.; Mueller, R. T.; Romney, E. M. 1973. Sodium relations

in desert plants: 2. Distribution of cations in plant parts of three

different species of Atriplex. Soil Science. 115:390–394.

Wilkins, S. D.; Klopateck, D. 1984. Moisture stress, Atriplex species

and reclamation at Black Mesa, AZ. In: Tiedemann, A. R.;

McArthur, E. D.; Stutz, H. C.; Stevens, R.; Johnson, K. L. comps.

Proceedings Symposium on the Biology of Atriplex and related

chenopods; 1983 May 2–6; Provo, UT. General Technical Report

INT-172 Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Forest and Range Experiment Station.

Yeo, A. R.; Flowers, T. J. 1986. Salinity resistance in rice (Oryza

sativa L.) and a pyramiding approach to breeding varieties for

saline soils. Australian Journal of Plant Physiology. 13:161–173.
312 USDA Forest Service Proceedings RMRS-P-21. 2001

Mata-González, Meléndez-González, and Martínez-Hernández Aerial Biomass and Elemental Changes in Atriplex canescens and A. acanthocarpa...
USDA Forest Service Proceedings RMRS-P-21. 2001 6

Community Ecology

313

USDA Forest Service Proceedings RMRS-P-21. 2001 315

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Suzanne Mayne is Range Management Specialist, Natural Resources

Conservation Service, 2047 N. Buckboard Drive, #4, Cedar City, UT 84720.

Neil West is Professor, Department of Rangeland Resources, Utah State

University, Logan, UT 84322-5230.

Field Test of a New Australian Method

of Rangeland Monitoring

Suzanne Mayne

Neil West

Abstract—Managers need more efficient means of monitoring

changes on the lands they manage. Accordingly, a new Australian

approach was field tested and compared to the Daubenmire method

of assessing plant cover, litter, and bare soil. The study area was a

2 mile wide by 30.15 mile long strip, mostly covered by salt desert

shrub ecosystem types, centered along the SE boundary of the Eagle

Bombing Range in NW Utah. Paired T analyses were used to see

what differences in condition could be detected between Bureau of

Land Management and U.S. Air Force lands occupying the same

ecological sites. Because of low statistical power of the test, no

statistically significant differences were detected between ownerships. We did however, find some numerical differences illustrating

the strengths and shortcomings of the two approaches. The Australian technique was less time consuming but not more readily

repeated than the Daubenmire technique. The Australian technique focuses on the importance of protecting soils against erosion.

The Daubenmire technique allows collection of data for addressing

biodiversity and weed invasion issues. Either or both methods

can be done on the same locations, thus, the managers’ objectives

and budgetary considerations should guide choices of method(s)

employed.

Introduction ____________________

Monitoring, while necessary for adaptive natural resource

management, can become expensive and tedious. The monitoring process on rangelands has traditionally involved

estimates of plant abundances in quadrats by species. Complete and accurate enumeration of abundance-weighted

species composition in samples from plant communities

requires practitioners who know the flora. Familiarity with

the flora requires training followed by experience. Universities are training fewer people with lower levels of competence in field botany than was the case in the past. Agencies

and other employers are offering fewer opportunities for

young professionals to gain further experience in learning to

identify plants. We, thus, need to explore additional ways to

monitor rangelands that do not require as much investment

in time to learn plant species as the traditional approach has

entailed.

Methods _______________________

During the summer of 1997, we gathered field data for

comparing a new Australian method (Tongway and Ludwig

1997) with a traditional approach (Daubenmire 1959) long

used to enumerate vegetation cover in the Intermountain

Region. Our study area was in northwestern Utah, along the

southeastern boundary of the North Unit (“Eagle Bombing

Range”) of the Utah Test and Training Range in Box Elder

and Tooele Counties, Utah. For a two mile wide by 30.15 mile

long transect along this boundary, we compared characteristics of vegetation and soil surfaces for ecological site

polygons (Creque and others 1999) that straddled the fence

line separating the land managed by the U.S. Air Force (AF)

from that controlled by the Bureau of Land Management

(BLM). The fence at this boundary had been constructed in

1968 and differing management pursued thereafter. Prior to

1968, livestock, mostly sheep, had grazed the land under

both current ownerships. Since livestock had been fenced

out of the AF property for nearly 30 years, we expected to find

higher (later seral) conditions on the AF side of the fence

because of the greater opportunity for the vegetation to

recover from livestock grazing impacts there.

Before we could evenhandedly sample the vegetation and

soil surfaces characteristics under the two ownerships, we

had to delineate polygons of relative high internal environmental homogeneity that could be expected to have the same

potentials for vegetation and responses to management. In

other words, the first step was to delineate ecological sites

(Creque and others 1999). We did this in the field with

conventional orthophotos (1:24,000 scale) taken between

1972 and 1978 (depending on the particular quadrangles

involved). Polygons delineating individual examples of ecological sites were drawn on acetate overlays and questionable boundaries checked on the ground. We didn’t distinguish polygons that were less than 5 ha in total size (the

minimum mapping unit). We also didn’t distinguish potential lobes of polygons less than 100 m in width. In other

words, if there were small but nearly symmetrical inclusions

of another possible ecological site within the polygon, these

were ignored in the delineation. The width criterion meant

that differing environments along bottoms of drainages or

ridgelines were also ignored. Since we needed adequate area

on both sides of the fence for reasonable sampling, we had to

identify those polygons representing a given ecological site

(ES) that straddled the fence and provided at least 5 ha area

on each side. Each potentially sampled piece of land also had

to extend at least 200 m along the same general slope in

order for the Australian method (requiring a 100 m transect)

to be accommodated with some buffer left for any disturbance created by fence building, fence maintenance, and

changes in animal behavior next to the fence. We found
316 USDA Forest Service Proceedings RMRS-P-21. 2001

Mayne and West Field Test of a New Australian Method of Rangeland Monitoring

23 such opportunities. Color-coded maps of the individual

polygons, the ecological site represented, and of our plot

locations can be found in Sharik (2000). These areas were

linked to the Natural Resources Conservation Service (NRCS)

soil survey (Trickler 1986) of the UTTR and later county soil

surveys of the adjacent BLM land by the NRCS. This process

led to the grouping of the 23 polygons meeting our criteria

into 4 of the commonest ecological sites. Nine comparisons

were made in the Desert Loam ES, five in the Desert

Gravelly Loam ES, five in the Desert Flat ES, and four in the

Alkali Flat ES. The sampled sites are all variants of the salt

desert shrub ecosystem type (West 1983).

The next step was select points to sample within the AF

and BLM portions of the large enough individual site polygons straddling the fence line. We examined the variation in

photographic texture across the paired portions of the polygon on the orthophotos and chose a location where texture

was both homogeneous and representative of the entire

polygon. We then went to that location in the field. Both plot

locations and polygon boundaries were entered into a geographic information system (Sharik 2000).

At each of the 46 transects (one per each side of the fence)

a 100 m tape was laid out down the prevailing slope. Along

these transects, two types of ground cover data were taken: by

the traditional Daubenmire and the new Australian method.

The Daubenmire approach involved placement of twentyfive 20 x 50 cm micro-plots at random points along one side

of the tape. Within the micro-plots, plant canopy cover

estimates were made by species using the cover classes

suggested by Daubenmire (1959).

Under the Australian method (Tongway and Ludwig 1997),

line intercepts of basal cover of only the perennial plants

were recorded. While Tongway and Ludwig (1997) recommend that these data be recorded by growth form category,

we recorded live plant cover by species as well. Litter was not

distinguished by what plant species it likely was derived

from. This approach yields some other attributes besides

basal cover. The amount of distance between patches of

perennial plants is termed “fetch length.” This is a proxy for

bare ground ignoring any ephemeral plants. The number of

patches intercepted was also recorded, as were the widths of

plant bases that were intercepted.

In order to gain a sense of repeatability in applying the two

methods, four pairs of transects (one representing each of

the four ecological sites encountered) were read by both

methods a second time the next day following the initial

reading.

Statistical analysis of the data derived from the Australian method was by the paired T method (Subcommittee

1962). A T-test for the results derived from the Daubenmire

method was not performed because these data were not

spatially independent from those of the Australian method

(the main focus of our investigation). Both types of data were

recorded along the same transect lines. The power of these

tests and sample numbers required to reach predefined

statistical adequacies were calculated by the methods suggested in Chapter 11 and Appendix A of Elzinga and others

(1998).

Range condition, derived only from the Daubenmire data,

was scored by two methods. First, the Grazing Lands Technology Institute (1997) method was used with reference to

the Utah Condition Guides (Natural Resources Conservation

Service 1998). A second approach, based on degree of dominance by native plants, as suggested by Anderson (1991),

was also employed. We also calculated the percent of the

encountered flora that were considered invasive. For the

listing of which species were considered weeds see Sharik

(2000).

Results and Discussion __________

Using the traditional (Daubenmire) approach showed

numerically higher average total cover by plants and less

bare ground on the AF than BLM side of the fence (table 1).

Shrub cover was slightly higher on the AF side, whereas

canopy cover of perennial herbs was identical (table 1).

Annual herb cover, bare soil, litter and soil cover by

microphytes (lichens, mosses, and algae) was nearly the

same on both sides of the fence (table 1).

Range conditions were apparently the same on both sides

of the fence using the traditional NRCS method (table 1).

The degree of invasion by exotics was slightly less on the AF

side. Since the Index of Naturalness is 100 minus the

percentage of invasion by exotics, the AF property sampled

has a higher value for this property as well.

The new Australian method didn’t yield total plant cover

data. It focuses instead on the basal cover of perennials,

whereas the traditional method assesses canopy cover by all

plants present at the time of sampling. It should be pointed

out that the leaves of most of the cool season herbs had

already shattered when the data were taken in July and

thus, had probably become greatly diminished from their

earlier stature. Warm season herbs were still growing in

July, however, and thus would have greater contributions to

cover if measured later.

We intuitively expected the Australian method to be more

repeatable than the traditional approach. This is because

the Australian approach focuses on the intercepted basal

cover of perennials. However, when there are numerous

small-sized perennials, it proved difficult for the same intercepts to be encountered during the second reading. Thus, the

eye adjustments required in the Daubenmire canopy cover

method may compensate for the inexactitudes of line intercept approach. The Australian method presents data bearing on the fragmentation of perennial cover (Kuehl and

others 2001), features not addressed by the traditional

method. For instance, the mean fetch length was greater on

the AF side of the fence (table 1). This means that there was

more distance between clumps of individual perennial plants

and their more durable litter there. In other words, more bare

ground in larger patches occurred on the AF side. Mean patch

width was greater on the BLM side (table 1). This suggests

that perennial plants were, on average, larger there.

None of the differences discussed above were statistically

significant at anywhere near conventional levels (table 1,

fourth column). This was because statistical power was low

(table 1, fifth column). In order to reach within 10 percent of

the true mean with a 90 percent chance of not making a Type

I error, we would have had to employ many more transects

per polygon (table 1, sixth column). This would have greatly

increased the cost of monitoring, especially for the traditional method. The Australian method is faster and focuses

only on the perennial cover, thus statistical adequacy could
USDA Forest Service Proceedings RMRS-P-21. 2001 317

Field Test of a New Australian Method of Rangeland Monitoring Mayne and West

be reached with fewer samples (table 1, sixth column).

Another advantage of the Australian method is that it is

based on a concept that allows scaling up to landscapes and

provides means of connecting the data to estimates of soil

erosion and nutrient conservation (Ludwig and others 2000).

Conclusions____________________

Choice of methods to use in monitoring of rangelands

should follow expression of what the land is being managed

for, balanced against costs and reliability of the method

employed. For instance, the Australian method assumes

that protection of the soil against erosion is the number one

land management issue. Tongway and Ludwig (1997) also

assume that ephemeral vegetation and microphytes (mosses,

lichens, algae) play no decisive role in protecting the soil.

Contrary to what Tongway and Ludwig (1997) assert, choosing this focus on soil protection is not a value-free choice, but

as much a moralistic decision as choice of any other condition

objective.

The Australian method does not involve creating a full

species list with any expression of their abundance for

example, cover. Without practitioners trained to identify

plant species, the best that can be done under the Australian

approach is an enumeration of a modest set of life form

categories for the perennials only. Thus, if differences in

species level biodiversity within the entire plant community

is something one desires to know, a more traditional approach must be employed. These kinds of data are required

to calculate indices of similarity to reference states such as

usually done by the Grazing Lands Technology Institute

(1997) or using the Index of Naturalness (or degree of

invasion that is its inverse) as suggested by Anderson

(1991). Keeping these traditional approaches in play will

require that universities keep introducing students to the

topic of plant taxonomy and that employers give their new

employees opportunities to improve upon those initial skills.

References _____________________

Anderson, J.A. 1991. A conceptual framework for evaluating and

quantifying naturalness. Conservation Biology 5:347–355.

Creque, J.A., S.D. Bassett and N.E. West. 1999. Viewpoint: delineating ecological sites. Journal of Range Management 52:

546–549.

Daubenmire, R.F. 1959. Canopy coverage method of vegetation

analysis. Northwest Science 33:43–64.

Elzinga, C.L., D.W. Salzer and J.W. Willoughby. 1998. Measuring

and monitoring plant populations. U.S. Dept. Interior, Bureau of

Land Management, Technical Reference 1730-1, Denver, CO.

Grazing Lands Technology Institute. 1997. National Range and

Pasture Handbook. U.S. Department of Agriculture, Natural

Resources Conservation Service, Washington DC.

Kuehl, R.O., M.P. McClaran and J. VanZee. 2001. Detecting fragmentation of cover in desert grasslands using line intercept.

Journal Range Management 54:61–66.

Ludwig, J.A., J.A. Wiens and D.J. Tongway. 2000. A scaling rule for

landscape patches and how it applies to conserving soil resources

in savannas. Ecosystems 3:84–97.

Natural Resources Conservation Service. 1998. Ecological Site

Guides for Utah. Salt Lake City, Utah.

Sharik, T.L. project coordinator, 2000. Final Report. Population,

Distribution, and Habitat Study for Threatened, Endangered,

and Sensitive Species of Plants and Animals Within the Hill Air

Force Base (HAFB) Restricted Air Space and Associated Public

Lands. GIS Data and text on CD-ROM. Remote Sensing/GIS Lab,

Utah State University, Logan.

Subcommittee on Range Research Methods of the Agricultural

Board. 1962. Basic Problems and Techniques in Range Research.

National Academy of Sciences—National Research Council,

Washington, DC.

Tongway, D.J. and J.A. Ludwig. 1997. The nature of landscape

dysfunction in rangelands. In: J. Ludwig, D. Tongway, D.

Freudenberger, J. Noble and K. Hodgkinson (eds.). Landscape

Ecology: Function and Management. Commonwealth Scientific

and Industrial Research Organization, Collingwood, Victoria,

Australia: 49–61.

Trickler, D.L. 1986. Air Force Base, Utah, Soil and Range Survey.

U.S. Department of Agriculture, Soil Conservation Service, Salt

Lake City, Utah.

West, N.E. 1983. Intermountain salt-desert shrublands. In: N.E.

West (ed.). Temperate Deserts and Semi-deserts. Vol. 5, Ecosystems of the World. Elsevier Sci. Publ. Amsterdam, Netherlands:

375–397.

Table 1—Summary of overall results obtained by the two methods on the two sides of the fence. BLM = Bureau of Land Management,

AF = Air Force, T = probability of a statistically significant difference with a chance of a type I error of one in ten. N = number of

samples, that would have to have been obtained for a statistically significance (p = 0.10) to have been obtained.

 BLM AF Difference T Power n

Daubenmire method (percent of ground covered)

 Shrub cover 14 16 2 0.135 370

 Perennial herb cover 2 2 0 0.057 1,811

 Annual herb cover 13 12 1 0.029 7,322

 Microphytic crusts 43 42 1 0.028 47,550

 Total plant cover 30 31 1 0.077 934

 Litter 4 4 0 0.928 26

 Bare ground 10 9 1 0.176 260

 Total 112 113 1 0.026 80,091

 Range condition 48 48 0 0.068 1,228

 Degree of weed invasion 36 33 3

 Index of naturalness 64 67 3

Australian method (per 100 m)

 Mean fetch length (cm) 580 910 321 0.309 0.156 304

 Percentage in fetches 5.8 9.1 33

 Mean patch number 26 24 2 0.096 0.037 463

 Mean total patch width (m) 4.3 3.4 0.9 0.612 0.116 463
318 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

K. T. Harper is Professor Emeritus of Botany and Range Science at

Brigham Young University, Provo, UT, and Scholar in Residence at Utah

Valley State College, Orem, UT. Stewart C. Sanderson is Research Geneticist

and E. Durant McArthur is Project Leader and Research Geneticist at the

Shrub Sciences Laboratory, Rocky Mountain Research Station, U.S. Department of Agriculture, Provo, UT 84606

Abstract—The vegetation of Zion National Park (ZNP) is used to

illustrate the use of various indices that describe aspects of

botanical diversity. The simplest method reports the average number of vascular species per 0.01 ha (0.025 acre) macroplot. The

MacArthur-Wilson index of diversity is given for each plant community of occurrence in the Park. Neither the number of species per

macroplot nor the MacArthur-Wilson index show much variation

among the plant communities of the Park. A third index shows the

proportion of a community’s major species that reach maximum

regional abundance in that community. This index records large

differences among communities and is indicative of the amount of

genetic diversity inherent in a community. Such information will be

of interest to evolutionists, plant breeders, and horticulturists. A

fourth index quantifies the degree to which major species of a

community are rare elsewhere in the region. This rarity index also

shows large differences among the communities considered. Since

rarity has unusual appeal to humans, this index identifies communities of particular interest to users and managers. Vegetational

composition upon which all indices are based is reported for the 10

major communities of ZNP. Procedures for computing each index

are given.

Most conservation efforts of the past have focused on

individual species. Such activities have emphasized the life

cycle, reproductive biology, and habitat requirements of

individual species. Those studies have often resulted in

greatly enlarged populations and improved habitat for species in danger of extinction. Nevertheless, conservationists

have increasingly called for preservation of entire biotic

communities and habitats associated with them (Owen and

others 1998).

A large literature has developed around the general theme

of preservation of individual species. Included are rigorous

methods for quantifying genetic diversity of individuals and

populations, for estimating population size, and for evaluating the likelihood of extinction in future time periods of

variable length (Primack 1998). In contrast, little attention

has been directed to procedures for quantifying the degree to

which various natural communities are threatened, the

Quantifying Plant Diversity in Zion National

Park, Utah

K. T. Harper

Stewart C. Sanderson

E. Durant McArthur

likelihood that they harbor rare species or contain unique

genotypes, or are the habitat of species vulnerable to extinction. Greater effort has been devoted to development of

procedures for describing characteristics of individual plant

communities (Whittaker 1975).

This paper represents an attempt to quantify various

aspects of the biodiversity of the plant communities of

Zion National Park (ZNP). Our analyses are based on a

large vegetational sample drawn from throughout ZNP,

an area that covers approximately 60,000 ha in southwestern Utah. Since the Park extends over an area of

variable geology and diverse topography, plant communities adapted to very different microenvironments are

represented in the sample.

Methods _______________________

Our sample is based on 0.01 ha macroplots placed at the

intersection of a 1.61 km (1.0 mile) grid across the entire

surface of ZNP. In all, 309 macroplots were thus sampled

within the Park. Since essentially the entire area of concern has been covered by the United States land survey, we

used U.S. Geological Survey, 7.5 min quadrangle, topographic maps to locate the site of each section corner in the

field. Workers visited each corner and delimited a circular

macroplot centered on the corner.

At each section corner (or as near that point as topography

would permit), a macroplot was inventoried using procedures similar to those developed by workers at the ZurickMontpellier School of Phytosociology (Braun-Blanquet 1932).

At each plot, all vascular species rooted therein were recorded and foliage cover (projected crown) of each was

visually estimated. Workers also recorded elevation, aspect,

and slope at each plot. Geologic substrate at the site, seral

state of the vegetation, and evidence of prior disturbing

influences (such as domestic grazers, logging, abandoned

roads or trails, wildfire, and so forth) on the plot were

recorded. Finally, the worker made an estimate of composition of the living cover (percentage of the total contributed by

lifeform groups such as trees, shrubs, perennial broadleavedherbs or graminoids, annuals, or nonvascular species) and

the abiotic surface (relative cover of bare soil, consolidated

rock, rock pavement, boulders, or litter).

Since some of the plant communities of occurrence within

ZNP are of very limited area there (for example, abandoned

fields, riparian forests, and hanging gardens), we have arbitrarily selected sampling points in those community types

that do not fall on section corners. All well-developed hanging gardens encountered that approached 0.01 ha in area

were sampled. Within the abandoned fields and riparian
USDA Forest Service Proceedings RMRS-P-21. 2001 319

Quantifying Plant Diversity in Zion National Park, Utah Harper, Sanderson, and McArthur

Table 1—Definitions of words or terms used to describe the various indices computed to characterize

aspects of plant diversity of the several plant communities recognized in Zion National Park.

Procedures for computing the four indices are also given.

Word or term Definition or computational procedures

Modal species Prevalent species that reach maximum regional commonness in the community

in question (Curtis 1959).

Percentage presence The percentage of all macroplots placed in each community type that included

rooted individuals of species X.

Prevalent species The commonest species in a particular community type selected in a number

equal to the species density for that community. All species encountered in the

full sample for a community are arranged in decreasing order of percentage

presence. Prevalents are selected from the top of that list in a number equal

to average species density for the community. The number is rounded up to the

nearest whole number (Curtis 1959).

Species density The average number of species occurring in the macroplots of any particular

community type (Curtis 1959).

Index Computation

Diversity Diversity (D) = 1/ ∑pi2 where p = the decimal proportion of the sum of percent

of presence of all prevalent species in the community contributed by each

prevalent species. D is an approximation of the number of species of equal

commonness in the community (MacArthur and Wilson 1962).

Distinctiveness Distinctiveness = no. modal prevalent species x 100 (Curtis 1959)

 no. prevalent species

Rarity The number of occurrences of each community prevalent in the entire study

(309 macroplots) is expressed as a decimal fraction of the total of plots observe

(309). The reciprocal of each fraction is taken. These reciprocal values are

summed across all prevalent species of any given community and their average

value is obtained. That average is taken as the rarity index for that community.

Table 2—The 10 plant communities recognized in Zion National Park, the gross characteristics of their environments, the relative area of each within

the Park, and sample size by community are presented here. Aspects of the soils associated with each community can be found in

Mortensen and others (1977).

Percent of Average Predicted annual Percent of coverage

Community Park area elevation (m) precipitationa (cm) of bare rock No. macro-plots

Blackbrush (CORA) 1.7 1,261 ~25.4 10.9 10

Abandoned fields 0.6 1,366 ~25.4 0.1 6

Riparian 1.5 1,490 ~25.4 12.6 19

Hanging gardens Trace 1,505 ~25.4 27.2 23

Sagebrush (ARTR) 2.4 1,510 ~32.6 4.9 7

Juniper- pinyon (JUOS-PIMO) 46.5 1,700 ~38.1 20.1 108

Rock crevice 19.1 1,770 ~38.1 60.6 25

Mountain brush 13.9 1,946 ~45.6 8.5 57

Ponderosa pine (PIPO) 8.3 1,970 ~45.6 14.2 33

Douglas-fir-white fir

 (PSME-ABCO) 6.1 1,997 ~50.8 9.3 21

a

Based on a regression equation developed by Harper (1993) using data from stations of known elevation and precipitation in the general region of ZNP.

community types, a stratified-random method was used to

select additional macroplot locations when section corners

within the type were few in number. Plant nomenclature

follows Welsh and others (1993).

Since our study utilized concepts and indices not commonly employed among land managers, we have provided a

list of terms and indices used as we prepared this manuscript. Words and terms are defined and procedures given

for computing the four indices that we use (table 1).

Results ________________________

We have recognized 10 plant communities in ZNP

(table 2). Criteria for recognition were those commonly

used by land managers in the area. Most of the community

types could be justifiably further subdivided, but such

fragmentation quickly results in sample sizes that are too

small to permit reliable statistical tests of differences
320 USDA Forest Service Proceedings RMRS-P-21. 2001

Harper, Sanderson, and McArthur Quantifying Plant Diversity in Zion National Park, Utah

observed between subunits. We have elsewhere (Harper

1993) suggested habitat-type subdivisions for the major

communities that are likely to be useful for management.

The communities recognized in the Park range in elevation from an average of 1,261 m (blackbrush or Coleogyne

ramosissima community) to almost 2,000 m (Douglas-fir/

white fir or Pseudotsuga menziesii/Abies concolor forests).

Precipitation averages from about 25 cm per year in the

blackbrush shrub deserts to over 50 cm per year in the mixed

conifer forests (table 2). Since the Park covers an area of

rugged, rapidly eroding terrain, most of the plant communities occur on very rocky sites. The rock crevice community,

as recognized here, averaged over 60 percent of bare rock on

constituent sites, and only four communities showed less

than 10 percent bare rock (table 2).

The commonest communities in the Park were juniperpinyon (46.5 percent of the surface area of the Park), rock

crevice (19.1 percent of the Park), and mountain brush (13.9

percent). Five communities individually covered less than

3.0 percent of the area of the Park: uncommon communities

arranged in order of increasing area included hanging gardens, abandoned fields, riparian, blackbrush, and sagebrush (table 2).

We summarize data for occurrence (percent presence in

the macroplots of each community type) of all prevalent

species in the 10 communities recognized in the Park in

table 3. Although 929 plant taxa have been collected in ZNP

[based on a checklist prepared by Kaye Thorne (1989) and

collections made during the course of the field work for this

report], only 514 taxa occurred in the macroplots inventoried

Table 3—Prevalent species performance in 10 plant communities of Zion National Park. The values reported are percentage occurrence in the

0.01 ha (0.025 acre) macroplots placed in each community. Values are underlined in communities where the species is prevalent and

underlined and bold where the species are both prevalent and modal. See table 1 for definitions of the terms prevalent and modal. All

results reported here are derived from a report by Harper (1993).

Aband. Hang. JUOS Rock. Mt. PSME

Species CORA fields Riparian garden ARTR PIMO crev. brush PIPO ABCO

Woody

Abies concolor 16 20 4 5 52

Acer grandidentatum 37 40 1 14 6 43

A. negundo 63 60 4 2 10

Amelanchier utahensis 40 14 65 56 49 64 62

Arctostaphylos patula 5 20 38 60 35 61 10

Arenaria macradenia 11 16 18 24 19

Artemisia tridentata 10 5 100 26 19 18

Atriplex canescens 33 14 1

Cercocarpus intricatus 5 20 5 84 7 21 24

Chrysothamnus nauseosus 20 17 16 43 13 16 16 12 5

Coleogyne ramosissima 100 5 2

Ephedra nevadensis 40 9 4

Fraxinus anomala 5 20 27 12 12 29

F. velutina 32

Gutierrezia microcephala 80 50 21 20

G. sarothrae 71 44 36 21 21

Haplopappus scopulorum 14 19 4 12 15 38

Holodiscus dumosus 16 20 32 2 3 33

Juniperus osteosperma 60 33 20 14 82 12 19 18

J. scopulorum 5 20 1 19 9 24

Lycium pallidum 33

Mahonia repens 16 20 6 12 12 38

Opuntia macrorhiza 30 11 29 53 56 44 49 24

O. phaeacantha 17 29 2 53

Pachystima myrsinites 11 60 12 4 23 24 71

Petrophytum caespitosum 5 39 28 3 10

Pinus edulis 20 34 4 12 15 19

P. monophylla 40 5 53 12

P. ponderosa 5 20 2 56 11 97 29

Phlox austromontana 5 14 15 20 30 39 5

Populus fremontii 32

Pseudotsuga menziesii 11 40 423 48

Psorothamnus fremontii 30 14 5

Purshia tridentata 5 20 14 4 19 30 5

Quercus gambelii 17 37 60 34 24 75 67 86

Q. trubinella 5 30 32 16 12

Symphoricarpos oreophilus 11 13 4 46 18 52

Tamarix ramosissima 21 14

Yucca angustissima 5 17 20 14 24 10

(con.)
USDA Forest Service Proceedings RMRS-P-21. 2001 321

Quantifying Plant Diversity in Zion National Park, Utah Harper, Sanderson, and McArthur

Monocotyledonus herbs

Agrostis stolonifera 28

Aristida purpurea 10 33 5 14 11 24 2 9

Bromus ciliatus 17 37 20 2 14

B. diandrus 17 42 2

B. rubens 80 17 25 12 5 3

B.tectorum 70 100 47 86 54 24 37 33 10

Calamagrostis scopulorum 79

Calochortus flexuosus 40 2

Carex curatorum 28

C. rossii 5 20 13 48 26 42 57

Elymus elymoides 20 11 57 26 12 14 9 10

Hilaria jamesii 60 17 43 22 4 4

Muhlenbergia thurberi 33 32

Poa bigelovii 30 3 2

P. fendleriana 17 47 14 69 84 74 85 71

P. pratensis 21 1 7 6 14

Sporobolus cryptandrus 20 67 21 29 11 12 26 12 5

Stipa hymenoides 40 21 20 29 32 16 19 9 5

Vulpia octoflora 70 17 16 43 35 44 14 24 5

Dicotyledonous Herbs

Antennaria rosulata 20 1 2

Apocynum androsaemifolium 40

Aquilegia chrysantha 50

A. formosa 50

Arabis perennans 20 32 57 36 47 36 38

Arenaria fendleri 64 7 18

Artemisia dracunculus 33 14 2 11 3

A. ludoviciana 17 42 20 17 12 25 12 14

Aster glaucodes 5 40 2 2

A. herperius 72

Astragalus nuttallianus 40 4

Castilleja scabrida 60

Chaenactis douglasii 18 36 12 30 10

Cirsium arizonicum 26 3879

Comandra umbellatum 11 16 19 24 10

Cryptantha (unknown annual) 50 14 32 32 18 12

C. confertiflora 36

Descurainia pinnata 40 29 18 5 5

Dodecatheon pulchellum 44

Draba asprella 16 20 4 32 11 15 38

D. verna 50 11 14 21 12 9 6

Eriastrum eremicum 30 3

E. spariflorum 10 5 29 7

Erigeron canaani 5 28 4 9 24

E. divergens 29 8 59

E. sionis 10 29 20 12 5

E. utahensis 39

Eriogonum palmerianum 50 8 2

E. racemosum 10 26 20 16 16 33 27 24

Erodium cicutarium 10 50 14

Erysimum asperum 11 27 8 32 30 19

Eupatorium herbaceum 21 40 2 19

Euphorbia albomarginata 10 67 11 20 14 9 4 6

Gilia inconspicua 90 11 49 16 25 12

Heterotheca villosa 33 37 20 14 14 64 32 49 10

Heuchera rubescens 11 8 2 29

Lactuca serriola 50 16 14 3 4

Lobelia cardinalis 56

Machaeranthera canescens 5 11 8 32 15 5

Mimulus cardinalis 72

Oenothera pallida 33 4

Pectocarya setosa 29 1

Table 3 (Con.)

Aband. Hang. JUOS Rock. Mt. PSME

Species CORA fields Riparian garden ARTR PIMO crev. brush PIPO ABCO

(con.)
322 USDA Forest Service Proceedings RMRS-P-21. 2001

Harper, Sanderson, and McArthur Quantifying Plant Diversity in Zion National Park, Utah

Table 3 (Con.)

Aband. Hang. JUOS Rock. Mt. PSME

Species CORA fields Riparian garden ARTR PIMO crev. brush PIPO ABCO

Penstemon humilis 36

P. laevis 40

P. rostriflorus 26 7 28 18 6 19

Phacelia heterophylla 26 20 8 12 32 9 19

Polygonum douglasii 7 12 28 33 14

Senecio multilobatus 16 20 36 40 46 52 33

S. spartioides 37 29 4 14 9 14

Smilacina stellata 33

Solidago sparsiflora 26 40 1 28 21 18 19

Stellaria jamesiana 5 18 3 29

Sphaeralcea grossularifolia 33 5 2

Stephanomeria tenuifolia 32 20 13 48 18 24 19

Streptanthus cordatus 10 31 4 10

Thelypodium laxiflorum 21 145

Tragopogon dubius 67 435

Vicia americana 5 20 10 28 12 48

Zauchneria latifolia 26 1 12 4 6 14

Nonseed plants

Adiantum capillus-veneris 89

Cystropteris fragilis 21 20 2

Equisetum hyemale 17 26 20 3

No. prevalent species 19 16 22 23 14 22 24 23 22 22

No. modal species 17 12 11 18 8 7 13 4 10 16

No. prevalents encountered 32 25 66 48 32 81 64 83 65 60

for this study. Furthermore, only 117 different species were

recognized as prevalent species in the 10 communities of

concern (table 3). These data emphasize that most species in

the flora of ZNP are uncommon. Only seven species occurred

in over 100 macroplots. In order of decreasing commonness,

those species are Poa fendleriana (189 macroplots),

Amelanchier utahensis, Quercus gambelii, Bromus tectorum,

Arabis perennans, Opuntia macrorhiza, and Juniperus

osteosperma (115 macroplots). All are native perennials

with the exception of Bromus tectorum, which is both an

annual and an alien to North America. Woody species are

over-represented in this group of seven common species,

since woody taxa account for only 19.6 percent of the species

of occurrence in the full flora of the Park.

The data (table 3) show that only Bromus tectorum was a

prevalent species in seven plant communities. Another five

species were prevalents in six different plant communities.

That group of broadly adapted, abundant species consisted

of Amelanchier utahensis, Opuntia macrorhiza, Quercus

gambelii, Poa fendleriana, and Arabis perennans.

The vast majority of prevalents (71 species) were so

narrowly adapted that they were designated as prevalent

species in a single community only. Such data further

emphasize that most species are uncommon in any region.

Analysis shows that woody species are significantly more

likely to be prevalent (39 of 117 prevalents) than one would

expect by chance given the incidence of woodiness in the

Park flora (19.6 percent of the 929 taxa). Wind pollinated

taxa are also significantly more likely to be prevalents (39 of

117 prevalents) than expected by chance, since only 23.4

percent of the taxa in the flora were considered to be wind

pollinated. Alien species were about equally represented

in the Park flora (9.8 percent) and among the prevalents

(9 taxa) listed in table 3.

In table 4, we present values for four different indices

considered to reflect diversity or rarity characteristics inherent in each plant community considered. It is immediately clear that neither the average number of species per

macroplot nor the MacArthur-Wilson diversity index show

much difference among the 10 plant communities. By both

indices, sagebrush and abandoned field communities have

the lowest values observed for the 10 communities.

In contrast, both the distinctiveness index and especially

the rarity index show large differences among the communities considered (table 4). The distinctiveness index indicates

the percentage of prevalents species achieve maximum

regional commonness in that community. Three communities show less than 40 percent of their prevalents reaching

maximum regional abundance in that community (the mountain brush, ponderosa pine, and juniper-pinyon communities). Other communities such as hanging gardens,

blackbrush, and abandoned fields have over 80 percent of

their prevalents achieving maximum regional commonness

in that community (table 4).

The rarity index shows low values for the juniper-pinyon,

mountain brush, ponderosa pine, rock crevice, and Douglasfir-white fir communities (table 4). Low rarity scores indicate that few of the prevalent species in a community are

otherwise rare in the region. Three communities (hanging

gardens, sagebrush, and abandoned fields) had very high

values for the rarity index. High rarity values arise when

many of the commonest species in the community are uncommon in all other communities in the region.
USDA Forest Service Proceedings RMRS-P-21. 2001 323

Quantifying Plant Diversity in Zion National Park, Utah Harper, Sanderson, and McArthur

Discussion _____________________

The prevalent species concept as formulated by Curtis

(1959) provides an objective method for identifying the

important species of any particular community. Since there

are usually more species encountered in large samples of

any community than one can list and discuss within the

space limitations of a published report, there is a definite

need for an objective method for selecting a manageable

number of species representative of any community type. By

focusing on the commonest species, as the prevalent species

concept does, one identifies those species from the regional

flora that are best adapted to the unique environments

associated with a particular community type. Our experience has demonstrated that one is often unable to identify

any behavior characteristic that is statistically over- or

under-represented in a given community type relative to the

representation of that character in the regional flora, when

every species encountered in the community sample is used

for the test. However, when such tests are based upon

prevalent species, various behavioral traits (such as plant

longevity, pollinating agent, or lifeform-class) can be demonstrated to diverge significantly from their commonness in

the regional flora. Apparently, species that survive only in

rare microsites within a community or that represent chance

introductions that will not long survive in the community

weaken analyses based upon all species encountered in a

sample.

The foregoing discussion illustrates the desirability of

simultaneously studying the entire flora and the full vegetational complex of an area. Without a regional checklist of

species occurring in a region, one cannot determine whether

any particular plant characteristic is being selected for or

against in a particular environmental complex. However,

when both a regional checklist and prevalent species list

exists for a particular community types in that region, it is

possible to use Chi-square tests to determine whether a

given plant character is over- or under-represented in a

particular community. In ZNP, for example, the checklist

shows that 236 of the 929 species in the Park are annuals or

biennials. In the lowest elevation and driest plant community (blackbrush), 10 of 19 prevalent species are annuals. A

Chi-square test suggests that the annual habit is significantly over-represented in the blackbrush community, given

the incidence of annuals in the regional flora (SX2 value =

10.4, p < 0.01). By contrast, annuals are significantly less

common than one would expect by chance (none of the 22

prevalents are annuals) in the Douglas-fir-white fir community, the highest elevation community in ZNP (SX2 value =

7.4, p < 0.01).

Although Curtis (1959) made no inferences about genetic

variability and modal species, we suggest that modal species

are likely to harbor more genetic diversity than non-modal

species in the community of modality. We draw that inference from the fact that the origin of new mutations is directly

proportional to the size of a population (Dobzhansky 1951).

In addition, as Wright (1931) theorized, the rate of gene loss

by “drift” from a population is inversely proportional to

population size. Consequently, we suggest that genetic diversity should be greatest for a species where it is modal

(regionally most common). Furthermore, those communities in which a large percentage of the prevalents are also

modal (that is, community distinctiveness is high) are likely

to harbor more genetic diversity (summed across all constituent species) than communities having low distinctiveness indices (see table 1 for definitions). Again, Curtis

(1959) makes no connection between community distinctiveness and genetic diversity inherent in a community,

but we suggest that such a correlation is likely.

The rarity index varies in magnitude according to the

degree to which species common (prevalent) in one community are uncommon in other communities of the region. Since

rarity is of unusual interest to many users of plant communities, managers would benefit from an index that objectively quantified the amount of rarity in communities. The

rarity index of table 1 provides a means for ranking local

communities in respect to the degree to which they harbor

species that are elsewhere uncommon in the region. Since

the index is based on prevalent species, it also identifies

those communities in which regionally uncommon species

maintain larger populations and are likely to generate and

conserve genetic diversity important for their continued

persistence in the region.

Table 4—Four indices reflective of phytodiversity or species rarity are presented here for the 10 major plant

communities of Zion National Park.

Indices

Average no. species MacArthur-Wilson

Plant community per macroplot diversity Distinctiveness Rarity

Blackbrush 19 17.4 81 14.4

Abandoned fields 16 14.8 82 29.3

Riparian 22 17.5 60 18.3

Hanging gardens 23 20.8 96 37.2

Sagebrush 14 12.8 53 31.8

Juniper-pinyon 22 19.5 39 4.0

Rock crevices 24 20.9 54 6.8

Mountain brush 23 18.2 17 4.4

Ponderosa pine 22 18.1 38 4.5

Douglas-fir-white fir 22 19.1 60 8.5
324 USDA Forest Service Proceedings RMRS-P-21. 2001

Harper, Sanderson, and McArthur Quantifying Plant Diversity in Zion National Park, Utah

Finally, we acknowledge that the distinctiveness and the

rarity indices are positively correlated, but their relationship is sufficiently diffuse that we recommend that both be

used to describe plant communities. In respect to distinctiveness for example, the sagebrush community ranked seventh

from the top, but by the rarity index, sagebrush communities

rank second from the top. Both indices provide information

useful to managers, and since their values sometimes differ

markedly for the same community, we recommend that both

be used to describe communities.

Acknowledgments ______________

This work was funded, in part, by Zion National Park, U.S.

Department of the Interior. We thank Gay A. Harper and

Donna Barnes for assistance in manuscript preparation.

References _____________________

Braun-Blanquist, J. 1932. Plant sociology; the study of plant communities (English translation). New York, NY: McGraw-Hill.

Curtis, J. T. 1959. The vegetation of Wisconsin. Madison, WI: The

University of Wisconsin Press. 657 p.

Dobzhansky, Theodore. 1951. Genetics and the origin of species, 3rd

ed. New York, NY: Columbia University Press.

Harper, Kimball T. 1993. Zion National Park vegetation: Summary

report. Springdale, UT: Zion National Park.

MacArthur, R. H.; Wilson, E. O. 1967. The theory of island biography. Princeton, NJ: Princeton University Press.

Mortensen, Vearl L.; Carley, James A.; Crandall, Gordon C.;

Donaldson, Karl M., Jr.; Leishman, Garth W. 1977. Soil survey of

Washington County area, Utah. U.S. Department of Agriculture,

Soil Conservation Service and U.S. Department of the Interior,

Bureau of Land Management and National Park Services in

cooperation with Utah Agricultural Experiment Station. 140 p.

plus 94 maps.

Owen, Oliver S.; Chrias, Daniel D.; Reganold, John P. 1998. Natural

resource conservation, 7th ed., Upper Saddle River, NJ: Prentice

Hall. 594 p.

Primack, Richard B. 1998. Essentials of conservation biology, 2nd

ed. Sunderland, MA: Sinauer Associates. 659 p.

Thorne, Kaye H. 1989. Zion National Park vascular plant list.

Unpublished typescript on file at Stanley L. Welch Herbarium,

Provo, UT; Brigham Young University.

Welsh, S. L.; Atwood, N. D.; Goodrich, S.; Higgins, L. C., eds. 1993.

A Utah flora, 2nd ed., revised. Provo, UT: Print Services, Brigham

Young University. 986 p.

Whittaker, Robert H. 1975. Communities and ecosystems, 2nd ed.

New York, NY: MacMillan Publishing Co. 385 p.

Wright, Sewall. 1931. Evolution in Mendelian populations.

Genetics. 16:97–159.
USDA Forest Service Proceedings RMRS-P-21. 2001 325

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Wendy Rosler is a continuing Student at Brigham Young University,

Provo, UT. Janet G. Cooper is a retired Biology Teacher at Provo High School,

Provo, UT. Renee Van Buren is an Assistant Professor, Department of

Biology, at Utah Valley State College, Orem, UT. Kimball T. Harper is a

Professor Emeritus at Brigham Young University, Provo, UT.

Abstract—“The Box” is a canyon located in the western portion of

Box-Death Hollow Wilderness Area, Garfield County, southern

Utah. The objectives of this study included: (1) collect, identify and

make a checklist of the species of vascular plants found in “The

Box,” (2) search for threatened and endangered species within the

area, (3) provide an opportunity for high school students to develop

research skills that contribute to the reservoir of scientific information. During a period of 2 years, students of the Provo High School

Botany Club, the club advisor, and others collected and identified

304 species in 63 families. Twenty plant taxa collected during this

study had not previously been reported for Garfield County, UT.

Species-area relationships at this area are compared to selected

locations in Utah.

“The Box” is a north-south trending canyon which begins

in an aspen-fir forest near “Hells Backbone” road at an

elevation of 2,450 m in the Box-Death Hollow Wilderness

area, Garfield County, Utah. From this elevation the forest

gradually slopes downward to the riparian community adjacent to Pine Creek. Pine Creek is a clear, fast flowing stream

of moderate size. The stream flows through a canyon of

sandstone walls that become progressively higher and closer

together, forcing the stream-side trail to cross the creek over

40 times. It is impossible to hike through the 16 km canyon

without doing some wading. The southern end of the canyon,

at 2,040 m, opens to a relatively level pinyon-juniper-sagebrush community seven miles north of Escalante, Utah. The

Pine Creek gaging station is located near the canyon mouth.

The rocks of the canyon are sedimentary and of Jurassic

and Cretaceous age. The soils are derived primarily from

sandstone. They include such soil type as the Mikim clay

loam, Yarts sandy loam and Mepsum loamy fine sand

(Stokes 1986).

The warmest month is July with an average temperature

of 22.4EC. The coldest month is January with an average

temperature of –2.4EC. The average annual precipitation

for the period 1901 to 1996 totaled 25.5 cm at Escalante. An

average of 77.2 cm of snow falls each year at Escalante

(Pope and Brough 1986).

Plant Diversity at Box-Death Hollow

Wilderness Area, Garfield County, Utah

Wendy Rosler

Janet G. Cooper

Renee Van Buren

Kimball T. Harper

Under the direction of Janet Cooper, the Provo High

School Botany Club initiated this study in the fall of 1993.

During the following 2 years (1994 and 1995) five collection

trips were taken at different times of the year to provide a

reliable sample of the canyon’s flora. Each collection trip

emphasized a different section of the canyon, but on each

trip, specimens of species previously unknown in the area

were collected throughout the canyon. Plants collected were

either immediately identified and pressed or collected in

plastic bags and pressed as soon as the group arrived back

at camp. Identification and classification followed “A Utah

Flora” (Welsh and others 1993). “The Intermountain Flora”

(Cronquist and others 1989) was used as a supplementary

guide for plant identification.

This project provides the first thorough description of

the vascular flora occurring in the study area. The checklist of 304 species in 63 families is included in this report

as table 1. Twenty taxa on the list have not previously

been reported for Garfield County (table 2). The six largest families include: Asteraceae (50 species), Poaceae (36

species), Rosaceae (16 species), Scrophulariaceae (16 species), Fabaceae (15 species), and Brassicaceae (15 species).

Voucher specimens are deposited in the herbarium at

Utah Valley State College.

The relative area and floristic richness of the Box Wilderness area is compared with the same characteristics for

seven other locations in Utah (table 3). The relationship

between species and land area is graphically shown in

figure 1. The number of named plant taxa is somewhat

linearly related to the logarithm (base 10) of area sampled.

The regression of species on the area is statistically significant (p < 0.05), but the regression accounts for only slightly

more than 50 percent of the variation observed. Nevertheless, the regression line does serve a useful function in that

it shows locations that fall above (more species than expected for their area in this analysis) or below the regression

line. Locations falling below the line may be poorly collected

or have inherently low biodiversity. A reverse explanation

could be offered for locations falling above the regression

line.

Several points seem worthy of note in figure 1: (1) The Box

Wilderness study area appears to be quite thoroughly collected, since it is not unusually complex ecologically in this

suite of locations. (2) Two locations below the regression

line (the Desert Experimental Range and Tooele County)

are more arid than average for this set of locations and

somewhat less topographically variable. (3) Zion National

Park and Washington County fall far above the regression

line: both are topographically complex and well collected.
326 USDA Forest Service Proceedings RMRS-P-21. 2001

Rosler, Cooper, Van Buren, and Harper Plant Diversity at Box-Death Hollow Wilderness Area, Garfield County, Utah

Division Lycopodiophyta

Family Selaginellaceae

Selaginella mutica D. C. Eaton LB

Division Equisetophyta

Family Equisetaceae

Equisetum arvense L. LB, UB

Equisetum hyemale L. UB

Equisetum laevigatum A. Br.

Division Polypodiophyta

Family Polypodiaceae

Cystopteris fragilis (L.) Bernh. MB

Division Pinophyta

Family Cupressaceae

Juniperus communis L. UB,MB

Juniperus osteosperma (Torr.) Little LB

Juniperus scopulorum Sarg. LB

Ephedra viridis Cov. LB

Family Pinaceae (pine)

Picea pungens Engelm. LB,MB

Pinus edulis Engelm. LB, MB

Pinus ponderosa Lawson LB,MB

Pseudotsuga menziesii (Mirbel) Franco UB, MB

Division Magnoliophyta

Class Magnoliopsida

Family Aceraceae

Acer glabrum Torr. UB, MB

Acer negundo L. MB

Family Amaranthaceae

Amaranthus retroflexus L. LB

Family Anacardiaceae

Rhus aromatica Ait var. trilobata (Nutt.) Gray LB

Family Apiaceae

Angelica pinnata Wats. UB

Conioselinum scopulorum (Gray) Coult & Rose UB

Cymopterus lemmonii (Coult.& Rose) Dorn LB

Cymopterus purpureus Wats. LB

Ligusticum porteri Coult. & Rose UB

Lomatium latilobum (Rydb.) Mathias LB

Osmorhiza depauperata H. & A. UB

Family Apocynaceae

Apocynum androsaemifolium L. LB

Family Asclepiadaceae

Asclepias asperula (Decne.) Woodson LB

Family Asteraceae

Achillea millefolium L. UB

Ambrosia acanthicarpa Hook.

Antennaria neglecta Greene LB

Antennaria parvifolia Nutt. MB

Artemisia bigelovii Gray LB

Artemisia campestris L. LB

Artemisia carruthii Wood ex Carruth LB

Artemisia frigida Willd. LB

Artemisia ludoviciana Nutt. UB

Artemisia tridentata var. tridentata Nutt. LB

Aster ascendens Lindl. MB

Aster chilensis Nees UB

Aster foliaceus Lindl. in DC. var. parryi (D.C. Eaton) Gray UB

Aster glaucodes Blake UB

Aster occidentalis (Nutt.) T. & G. LB

Bahia dissecta (Gray) Britt.

Brickellia grandiflora (Hook.) Nutt.

Brickellia microphylla (Nutt.) var. scabra Gray LB

Table 1—Vascular plant checklist for “The Box”, Death Box Hollow Wilderness Area, Garfield County, UT. Sixty three families, 304 species. LB =

plants collected in the lower part of “The Box” (elevation 2,040 to 2,200 m); MB = plants collected in the middle part of “The Box” (elevation

2,200 to 2,500 m); UB = plants collected in the upper part of “The Box” (elevation >2,500 m).

Botanical name Location Botanical name Location

Chaetopappa ericoides (Torr.) Nesom LB

Chrysothamnus linifolius Greene LB

Chrysothamnus nauseosus (Pallas) Britt LB

var. arenarius (L.C. Anderson)

Chrysothamnus viscidiflorus (Hook.) Nutt. UB

Cirsium neomexicanum var. utahensis (Petrak) Welsh LB

Erigeron abajoensis Cronq. UB

Erigeron awapensis Welsh UB

Erigeron flagellaris Gray LB

Erigeron pumilus Nutt. LB

Gutierrezia sarothrae (Pursh) Britt. & Rusby UB

Helenium hoopesii Gray UB

Helianthella microcephala Gray LB

Heterotheca villosa (Pursh) Shinn. LB

var. hispida (Hook.) Harms

Hymenopappus filifolius Hook. LB

var. cinereus (Rydb.) Johnston

Hymenoxys acaulis (Pursh) Parker LB

var. arizonica (Greene) Parker

Hymenoxys acaulis (Pursh) parker var. nana Welsh LB

Hymenoxys richardsonii (Hook.) Cockerell UB

Iva axillaris L. UB

Machaeranthera bigelovii (Gray) Green

Machaeranthera canescens (Pursh) Gray

var. canescens UB,LB

Machaeranthera grindelioides (Nutt.) Shinn. LB

Psilostrophe sparsiflora (Gray) A. Nels. LB

Senecio douglasii DC. MB

Senecio eremophilus Richards. UB

Senecio multilobatus T. & G. UB

Senecio spartioides T. & G. var. spartioides LB

Stephanomeria spinosa (Nutt.) Tomb UB

Stephanomeria tenuifolia (Torr.) Hall LB

Taraxacum officinale Weber ex Wiggers UB

Tetradymia canescens DC. UB

Townsendia incana Nutt. LB

Tragopogon dubius Scop. LB

Family Berberidaceae

Mahonia repens (Lindl.) G. Don MB

Family Betulaceae

Betula occidentalis Hook. UB

Family Boraginaceae

Cryptantha confertiflora (Greene) Payson LB

Cryptantha fulvocanescens (Wats.) Payson LB

Cryptantha pterocarya (Torr.) Greene LB

Lappula occidentalis (Wats.) Greene LB

Lithospermum multiflorum Torr. ex A. Gray UB,LB

Lithospermum ruderale Dougl. ex Lehm LB

Mertensia arizonica Greene MB

Family Brassicaceae

Arabis demissa Greene MB

Arabis holboellii Hornem. var. pinetorum (Tidestr.) Rollins LB

Cardamine cordifolia Gray UB

Chorispora tenella (Pallas) DC. LB

Descurainia californica (Gray) Schulz LB

Descurainia richardsonii (Sweet) Schulz LB

var. sonnei (Robins.) C.L.Hitchc

Draba sp. UB

Lepidium montanum Nutt. var. jonesii (Rydb.) C.L. Hitchc. LB

Lesquerella intermedia (Wats.) Heller LB

Lesquerella ludoviciana (Nutt.) Wats. MB

Lesquerella rectipes Woot. & Standl. LB

(con.)
USDA Forest Service Proceedings RMRS-P-21. 2001 327

Plant Diversity at Box-Death Hollow Wilderness Area, Garfield County, Utah Rosler, Cooper, Van Buren, and Harper

Table 1 (Con.)

Botanical name Location Botanical name Location

Physaria newberryi Gray LB

Streptanthella longirostris (Wats.) Rydb LB

Streptanthus cordatus Nutt. ex T. & G. LB

Thlaspi montanum L. var. montanum LB

Family Cactaceae

Echinocereus triglochidiatus Engelm. LB

Opuntia fragilis (Nutt.) Haw. LB

Opuntia phaeacantha Engelm. LB

Opuntia polyacantha Haw. LB

Family Campanulaceae

Campanula parryi Gray LB

Campanula rotundifolia L. LB

Family Capparaceae

Cleome lutea Hook. LB

Family Caprifoliaceae

Lonicera involucrata (Richards.) Banks ex Sprengel UB

Sambucus caerulea Raf. LB

Sambucus racemosa L. MB

Symphoricarpos oreophilus Gray UB

Family Caryophyllaceae

Arenaria fendleri Gray LB

Arenaria macradenia Wats. LB

Stellaria longipes Goldie var. longipes UB

Family Chenopodiaceae

Chenopodium fremontii Wats. UB

Chenopodium graveolens LB

var. neomexicana (Aellen) Aellens

Chenopodium leptophyllum (Moq.) Wats. LB

Monolepis nuttalliana (Schultes) Greene LB

Salsola pestifer A. Nels. LB

Family Cornaceae

Cornus sericea L. UB, MB

Family Elaeagnaceae

Elaeagnus angustifolia L. LB

Shepherdia canadensis (L.) Nutt. UB

Shepherdia rotundifolia Parry LB

Family Ericaceae

Arctostaphylos patula Greene LB

Family Euphorbiaceae

Euphorbia brachycera Engelm. in Emory MB

Euphorbia micromera Boiss. LB

Family Fabaceae

Astragalus argophyllus Nutt. ex T. & G. LB

Astragalus ceramicus Sheldon LB

Astragalus kentrophyta Gray LB

Astragalus mollissimus Torr. LB

Astragalus subcinereus Gray LB

Astragalus utahensis (Torr.) T. & G. LB

Dalea searlsiae (Gray) Barneby. LB

Lotus utahensis Ottley LB

Lupinus sericeus Pursh LB

Medicago sativa L. LB

Melilotus albus Desr. ex Lam. LB

Melilotus officinalis (L.) Pallas LB

Oxytropis deflexa (Pallas) DC. var. sericea T. & G. UB

Thermopsis montana Nutt. in T. & G. LB

Trifolium repens L. UB

Family Fagaceae

Quercus gambelii Nutt. LB

Family Gentianaceae

Swertia radiata (Kellogg) Kuntze UB

Family Geraniaceae

Geranium caespitosum James LB, UB

Geranium richardsonii Fisch. and Trautv. UB

Geranium viscosissimum Fisch. and Mey. LB

Family Hydrophyllaceae

Phacelia ivesiana Torr. in Ives var. ivesiana LB

Family Lamiaceae

Mentha arvensis L. LB

Monardella odoratissima Benth UB

Family Malvaceae

Sidalcea candida Gray UB

Sphaeralcea coccinea (Nutt.) Rydb LB

Sphaeralcea parvifolia A. Nels. LB

Family Monotropaceae (Indian-pipe)

Pterospora andromeda Nutt. UB

Family Nyctaginaceae

Abronia fragrans Nutt. ex Hook LB

Boerhaavia spicata var. torreyana Wats. LB

Mirabilis linearis var. decipiens (Standley) Welsh

Mirabilis linearis (Pursh) Heimerl var. linearis LB

Mirabilis oxybaphoides (Gray) Gray in Torr LB

Family Oleaceae

Fraxinus anomala Torr. ex Wats. LB

Family Onagraceae

Epilobium angustifolium L. UB

Epilobium halleanum Hausskn. LB

Oenothera caespitosa var. marginata (Nutt.) Munz. LB

Oenothera flava (A. Nels.) Garrett var. flava UB

Oenothera pallida Lindl. LB

Family Plantaginaceae

Plantago patagonica Jacq. LB

Family Polemoniaceae

Gilia aggregata (Pursh) Sprengel MB

Gilia congesta Hook. var. frutescens (Rydb.) Cronq. LB

Leptodactylon pungens (Torr.) Nutt. LB

Linanthastrum nuttallii (Gray) Ewan LB

Linanthus bigelovii (Gray) Greene

Phlox pulvinata (Wherry) Cronq. LB

Phlox tumulosa Wherry LB

Family Polygalaceae

Polygala subspinosa Wats. LB

Family Polygonaceae

Eriogonum alatum Torr. in Sitgr. LB

Eriogonum cernuum Nutt. LB

Eriogonum palmerianum Reveal in Munz LB

Eriogonum racemosum Nutt. LB

Eriogonum subreniforme Wats. LB

Rumex patentia L. UB

Family Portulaceae

Portulaca oleracea L.‘ LB

Family Primulaceae

Androsace septentrionalis L. UB

Primula parryi Gray LB

Family Pyrolaceae

Pyrola chlorantha Swartz UB

Pyrola secunda L. UB

Family Ranunculaceae

Aconitum columbianum Nutt. in T. & G. UB

Actaea rubra (Ait.) Willd. UB

Clematis columbiana (Nutt.) T. & G. UB

Clematis ligusticifolia Nutt. LB

Ranunculus cymbalaria Pursh UB

Ranunculus inamoenus Greene UB

Ranunculus repens L. UB

Thalictrum fendleri Englem. ex Gray UB,MB

Family Rhamnaceae

Ceanothus fendleri Gray MB

(con.)
328 USDA Forest Service Proceedings RMRS-P-21. 2001

Rosler, Cooper, Van Buren, and Harper Plant Diversity at Box-Death Hollow Wilderness Area, Garfield County, Utah

Family Rosaceae

Amelanchier alnifolia (Nutt.) Nutt. UB

Amelanchier utahensis Koehne LB

Cercocarpus intricatus Wats. LB

Fragaria virginiana Duchesne UB

Geum macrophyllum Willd. UB

Holodiscus dumosus (Nutt.) Heller MB

Physocarpus alternans (Jones) J.T. Howell MB

Potentilla concinna Richards UB,MB

Potentilla crinita Gray UB

Potentilla fruticosa L. UB

Potentilla ovina Macoun UB

Prunus virginiana L. UB,MB

Purshia mexicana (D. Don) Welsh LB,MB

var. stansburyana (Torr.) Welsh

Purshia tridentata (Pursh) DC. MB

Rosa woodsii Lindl. LB

Rubus idaeus L. MB

Family Salicaceae

Populus angustifolia James LB,MB

Populus balsamifera L. var. trichocarpa (T. & G.) Brayshaw MB

Populus tremuloides Michx. UB,MB

Salix bebbiana Sarg. UB

Salix boothii Dorn MB

Salix brachycarpa Nutt. UB

Salix drummondiana Barratt in Hook. MB

Salix exigua Nutt. LB

Salix geyeriana Anderss. UB

Family Santalaceae

Comandra umbellata (L.) Nutt. LB

Family Saxifragaceae

Fendlerella utahensis (Wats.) Heller LB

Heuchera parvifolia Nutt. in T. & G. var. utahensis LB

Heuchera rubescens Torr. in Stansbury MB UB

Ribes cereum Dougl. UB,MB

Ribes inerme Rydb. UB,MB

Saxifraga odontoloma Piper UB,MB

Family Scrophulariaceae

Castilleja flava Wats.

Castilleja linariifolia Benth. LB

Castilleja scabrida Eastw. LB

Mimulus guttatus DC. UB

Orthocarpus purpureo-albus Gray LB

Penstemon barbatus (Cav.) Roth. UB

Penstemon breviculus (Keck) Nisbet & R. Jackson LB

Penstemon eatonii Gray LB

Penstemon linarioides Gray LB

Penstemon moffattii Eastw. LB

Penstemon ophianthus Pennell LB

Penstemon pachyphyllus LB

var. mucronatus (N. Holmgren) Neese

Penstemon strictus Benth. LB

Penstemon utahensis Eastw. LB

Veronica americana Schwein. ex Benth LB

Veronica arvensis L. UB

Family Urticaceae

Urtica dioica L. UB

Family Valerianaceae

Valeriana edulis Nutt. ex T. & G. UB

Family Violaceae

Viola adunca J.E. Sm. ex Rees UB

Viola nephrophylla Greene UB

Family Viscaceae

Arceothobium americanum Nutt. ex Engelm. in Gray LB

Arceuthobium divaricatum Engelm. LB,MB

Arceuthobium douglasii Engelm. UB

Phoradendron juniperinum Gray LB

Class Liliopsida

Family Agavaceae

Yucca harrimaniae Trel. LB

Family Commelinaceae

Tradescantia occidentalis (Britt.) Smyth LB

Family Cyperaceae

Carex aquatilis Wahl. LB

Carex praegracilis W. Boot. UB

Carex lanuginosa Michx. UB

Carex microptera Mack. UB,LB

Carex nebraskensis Dewey LB

Carex rossii F. Boott UB

Carex rostrata Stokes ex With. LB

Eleocharis palustris (L.) R. & S. LB

Family Iridaceae

Sisyrinchium demissum Greene LB

Family Juncaceae

Juncus arcticus Willd. LB, UB

Juncus ensifolius Wikstrom UB

Family Liliaceae

Allium cernuum Roth LB

Fritillaria atropurpurea Nutt. MB

Smilacina stellata (L.) Desf. LB, MB

Family Orchidaceae

Habenaria sparsiflora Wats. MB

Family Poaceae

Agropyron cristatum (L.) Gaertner var. desertorum LB

Agrostis stolonifera L. LB

Aristida purpurea Nutt. LB

Bouteloua gracilis (H.B.K.) Lag. ex Steudel LB

Bromus carinatus H. & A. UB

Bromus ciliatus L. UB

Bromus inermis Leysser UB

Bromus tectorum L. LB

Catabrosa aquatica (L.) Beauv. UB

Elymus elymoides (Raf.) Swezey UB

Elymus glaucus Buckley UB

Elymus hispidus (Opiz) Meld. UB

Elymus junceus Fisch. LB

Elymus smithii (Rydb.) Gould LB

Elymus trachycaulus (Link) Gould ex Shinn UB

Festuca octoflora Walter LB

Festuca ovina L. LB

Hilaria jamesii (Torr.) Benth. LB

Muhlenbergia andina (Nutt.) A. S. Hitchc.

Muhlenbergia asperifolia (Nees & Mey.) Parodi

Muhlenbergia richardsonis (Trin.) Rydb UB

Muhlenbergia thurberi Rydb. UB

Munroa squarrosa (Nutt.) Torr. LB

Poa compressa L. LB

Poa fendleriana (Steudel) Vasey LB

Poa nervosa (Hook.) Vasey UB

Poa palustris L. UB

Poa pratensis L. LB

Poa trivialis L. UB

Schizachyrium scoparium (Michx.) Nash in Small LB

Sporobolus cryptandrus (Torr.) Gray LB

Sporobolus flexuosus (Thurber) Rydb. LB

Stipa comata Trin. & Rupr. LB

Stipa coronata Thurber LB

Stipa hymenoides R. & S. UB

Stipa lettermanii Vasey UB

Table 1 (Con.)

Botanical name Location Botanical name Location
USDA Forest Service Proceedings RMRS-P-21. 2001 329

Plant Diversity at Box-Death Hollow Wilderness Area, Garfield County, Utah Rosler, Cooper, Van Buren, and Harper

Table 2—Species collected in “The Box”

that are new records for Garfield

County, Utah.

Astragalus argophyllus var. martinii

Boerhaavia spicata var. torreyana

Campanula rotundifolia

Chrysothamnus nauseosus var. arenarius

Cryptantha pterocarya var. pterocarya

Elymus glaucus

Epilobium hallaenum

Geranium viscosissimum

Habenaria sparsiflora var. laxiflora

Hymenoxys acaulis var. nana

Linanthus biglovii

Lithospermum ruderale

Lomatium latilobum

Opuntia phaeacantha var. phaeacantha

Penstemon barbatus

Phlox tumulosa

Poa compressa

Poa nervosa

Populus balsamifera

Rumex patentia

Salix drummondiana

Veronica arvensis

Table 3—Area and number of species and sub-specific taxa at each of

several locations in Utah. The literature source for the

information at each location is shown.

Number of

Location Area Families Genera Species

ha

Box Wildernessa 648 63 175 304

Desert Experimental Rangeb 22,543 42 134 240

Bryce Canyon National Parkc 15,092 73 232 458

Capitol Reef National Parkd 97,937 74 280 512

Zion National Parke 59,926 94 402 929

Kane Countyf 1,075,828 92 399 998

Tooele Countyf 1,914,592 84 380 881

Washington Countyf 584,121 110 556 1,374

aThis manuscript.

b

Goodrich (1986).

c

Spence and Buchanan (1993). dMeyer (1982).

e

Harper, Sanderson, and McArthur (2001).

f

Albee, Schulz, and Goodrich (1988).

y= -617.5 + 249.6X 

r = +0.729 ( p < .05) WACO

KACO ZNP

TOCO

CRNP BCNP

BOX DER

0

200

400

600

800

1000

1200

1400

1600

02468

log 10 Area

No. Species

sample pts.

Predicted Y

Figure 1—The relationship between area and plant

diversity at eight locations in Utah. (BCNP = Bryce

Canyon National Park; BOX = Box Wilderness study

area; CRNP = Capitol Reef National Park; DER = Desert

Experimental Range; KACO = Kane County; TOCO =

Tooele County; WACO = Washington County).

Acknowledgments ______________

This project was funded by a grant obtained by Dr. Eileen

Bunderson (deceased) of Brigham Young University. The

authors would like to thank: Dr. E. Bunderson, Delita

Barnett, Adam Froerer, Jana Gamette, Robyn Gamette,

Karin Holmes, Robert Holmes, Carly Rasmussen, Chad

Wright, and other members of the Provo High School Botany

Club for help with collection, pressing and identification of

specimens. Donna Barnes and Dianne Carter helped in

manuscript preparation.

References _____________________

Albee, Beverly J., Leila M. Schulz and Sherel Goodrich, 1988. Atlas

of the Vascular Plants of Utah. Utah Museum of Natural History,

Occasional Publication No. 7. 670 p.

Arnow, Lois A. 1971. Vascular flora of Red Butte Canyon, Salt Lake

County, Utah. Master of Science thesis. University of Utah. Salt

Lake City. 388 p.

Brough, Clayton R.; Pope, Dan, eds. 1996. Utah’s Weather and

Climate. Salt Lake City, UT. Publisher’s Press. 245 p.

Cronquist, A. and others. 1977–1994. Intermountain Flora (5 vols.

to date). The New York Botanical Garden, New York.

Goodrich, Sherel. 1986. Vascular Plants of the Desert Experimental Range, Millard County, UT; U.S. Department of Agriculture.

Forest Service. General Technical Report. INT-209. 72 p.

Harper, K. T.; Sanderson, S.; McArthur E. D. 2001. Quantifying

plant diversity in Zion National Park, Utah. In: McArthur, E. D.;

Fairbanks, D. J., comps. Shrubland ecosystem genetics and

biodiversity proceedings. 2000 June 13–15; Provo, UT. Proc.

RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station: 318–324.

Meyer, Susan E. 1982. Plant Checklist: Capitol Reef National Park.

Capitol Reef Natural History Association, Torry, Utah.

Spence, John R. and Hayle Buchanan. 1993. Checklist of the

Vascular Plants of Bryce Canyon National Park, Utah. Great

Basin Naturalist 53: 207-221.

Stokes, William Lee. 1986. Geology of Utah. Utah Museum of

Natural History, University of Utah and Utah Geological and

Mineral Survey, Salt Lake City.

Welsh, Stanley L.; Atwood N. D.; Goodrich S.; Higgins L. C. 1993. A

Utah Flora, 2nd ed. Printing Services, Brigham Young University,

Provo, UT. 986 p.
330 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Carl L. Wambolt is Professor of Range Science and Trista L. Hoffman was

a Graduate Assistant, Department of Animal and Range Sciences, Montana

State University, Bozeman, MT 59717.

Abstract—This study was conducted within the Gardiner Basin,

an especially critical wintering area for native ungulates utilizing

the Northern Yellowstone Winter Range. Mountain big sagebrush

plants on 33 sites were classified as large (≥22 cm canopy cover),

small (<22 cm canopy cover), or dead and then aged by counting

growth rings. Large and small plants averaged 32 and 6 years old,

respectively. Nearly half of the small plants were 5 years old, the

result of optimal conditions for establishment in 1988, the year large

wildfires burned much of Yellowstone National Park. Dead plants

averaged 41 years of age. A bimodal peak in establishment of

mountain big sagebrush corresponded with two large reductions in

the Northern Yellowstone elk population.

Introduction ____________________

Big sagebrush (Artemisia tridentataNutt.) grassland comprises the largest vegetation type in the Western United

States (Colbert and Colbert 1983) dominating 60 million ha

(Beetle 1960). Since the 1930s, control of sagebrush has been

a primary objective of many land managers, with the intent

of improving herbaceous production for livestock (Best 1972).

However, big sagebrush is recognized as valuable forage and

cover for many wild ungulates, (Kufeld and others 1973;

Welch and Peterson 1981; Wambolt and McNeal 1987;

Ngugi and others 1992; Wambolt 1996, 1998), birds, (Best

1972; Reynolds 1981; McAdoo and others 1989), and other

wildlife (Mullican and Keller 1986). Ironically, some land

managers are increasingly engaged in reducing big sagebrush, often for the stated purpose of benefiting wildlife.

There is much conjecture about the dynamics of big

sagebrush production, including the relationship with age.

Some believe that big sagebrush declines in production or

vigor after a certain age (West and others 1984), but details

and the interrelationships with environmental factors related to possible declines are unclear. Decadence, degradation, and senescence are terms commonly used in the

literature (Roughton 1972; Evans and Young 1978; Sinclair

1984) and in management plans relating to big sagebrush

Mountain Big Sagebrush Age Distribution

and Relationships on the Northern

Yellowstone Winter Range

Carl L. Wambolt

Trista L. Hoffman

(Anonymous 1979, 1982; Petroni 1991), but their relevance

to big sagebrush is vague. Our objective was to obtain an

understanding of the age distribution of mountain big sagebrush (Artemisia tridentata ssp. vaseyana [Rydb.] Beetle)

over a range of environmental conditions on 33 sites on the

Northern Yellowstone Winter Range (NYWR).

Methods _______________________

Study Area

The study was conducted in the Gardiner Basin of the

NYWR adjacent to Yellowstone National Park (YNP) in

southwestern Montana (fig. 1). Along the Yellowstone River

annual precipitation averages 305 mm. The nearby

benchlands receive 406 mm of precipitation. Half of the

annual precipitation is in the form of snow and June is the

wettest month. The Gardiner Basin is a natural winter

range for ungulates due to the orographic effects on precipitation of mountain peaks up to 3,353 m (Wambolt 1996). Elk

(Cervus elaphus nelsoni) and mule deer (Odocoileus hemionus

hemionus) are the important ungulates on the study area.

Glacial scouring and deposition have been strong influences on the soils. Parent materials include granites and

limestones deposited by glaciers as well as basalts and

breccias. The soil regolith in the study area may range from

a few cm in areas scoured by glaciers to over 1.5 m in

depositional areas. Mollisols are the dominant soil order.

Soil textures are most commonly loams and sandy loams

(Wambolt and McNeal 1987).

Four sagebrush taxa, basin big sagebrush (Artemisia

tridentata Nutt. ssp. tridentata), Wyoming big sagebrush

(A.t. ssp. wyomingensis Beetle and Young), mountain big

sagebrush, and black sagebrush (A. nova Nels.), occur sympatrically but with varying frequency. Mountain big sagebrush is the dominant on the majority of the area. Threadleaf

rubber rabbitbrush (Chrysothamnus nauseosus ssp.

consimilis [Green] Hall & Clem.), mountain low rabbitbrush

(C. viscidiflorus ssp. lanceolatus [Nutt.] Hall & Clem.),

narrowleaf low rabbitbrush (C.v. ssp. viscidiflorus var.

stenophyllus [Hook] Nutt.), and gray horsebrush (Tetradymia

canescens D.C.) occur throughout the sagebrush-dominated

portions of the area.

Bluebunch wheatgrass (Agropyron spicatum [Pursh.]

Scribn.) and Idaho fescue (Festuca idahoensisElmer) are the

principal grasses found as sagebrush understory. Other

common grasses are prairie junegrass (Koeleria macrantha

Ledeb.), needle-and-thread (Stipa comata Trin.& Rupr.),

and Indian ricegrass (Oryzopsis hymenoides [R. & S.] Ricker).
USDA Forest Service Proceedings RMRS-P-21. 2001 331

Mountain Big Sagebrush Age Distribution and Relationships on the Northern Yellowstone Winter Range Wambolt and Hoffman

Sampling

Each study site was a stand of mountain big sagebrush

that was relatively homogenous in characteristics such as

slope, aspect, and elevation. Confirmation of the mountain

big sagebrush subspecies was made in the lab using an

ultraviolet light (Stevens and McArthur 1974). Each study

site was at least 0.25 ha in size (40 x 60 m) and ranged up to

3 ha.

Measurements of plant parameters began near the end of

June 1993. The majority of sagebrush growth for the year

occurred before this time. Long shoots and leaves were fully

elongated, and an annual growth ring was well established

in the stem xylem. Therefore, measurable production increases by sagebrush plants were not expected over the

remainder of the summer. The plant parameters recorded

included browse form class, percent cover of live and dead

sagebrush, density of large, small and dead plants, percent

dead crown, age, and production of winter forage.

Browse form classes used were described by Wambolt and

others (1994). Plants that receive repeated heavy browsing

develop a dense canopy and a hedged appearance. Lightly

browsed plants have a more open canopy with linear growth

due to the annual extension of terminal leaders. Usually, all

of the plants on a site exhibited nearly the same browse form

class.

At each site, two line transects, 30 m long, were established with the slope to measure cover. The transects were

parallel to one another and 10 m apart. Belt transects of 60

m2 were established to obtain the other parameters by

measuring 1 m on each side of the line transect. Measurements from the transects were pooled.

A plumb bob was used to determine live and dead cover to

the nearest cm along the line transects. Live cover included

any leaves, leaders, stems or seedheads that intercepted the

line transect. Dead cover referred to the intercept of dead

sagebrush branches elevated above the ground.

Plant density was determined by counting all sagebrush

plants rooted within the belt transect. Plants were divided

into large, small and dead categories. A large plant measured >22 cm across the widest portion of its crown. This

minimum measurement was adapted from the sagebrush

production models used (Wambolt and others 1994). Plants

<22 cm were not considered to be significant contributors to

site production, but were important as representatives of

the younger age classes. Dead plants were separated from

woody litter by the requirement of at least one main stem

still rooted in place, and some portion of the stem remaining

above the ground. An ocular estimate of the percentage of

dead crown area was made for each large sagebrush. Estimates were made to the nearest 10 percent.

Figure 1—The Northern Yellowstone Winter Range. This study was conducted north of Yellowstone National Park in the

Gardiner Basin. That area is especially important for wintering ungulates.

Dome Mtn.

Winter Range

Gardiner 

Basin

16 km
332 USDA Forest Service Proceedings RMRS-P-21. 2001

Wambolt and Hoffman Mountain Big Sagebrush Age Distribution and Relationships on the Northern Yellowstone Winter Range

Production was defined after Wambolt and others (1994)

as the amount of sagebrush forage available to wildlife

during winter. Production measurements were made on 10

large plants per line transect. The 10 plants were those

rooted closest to 3 m increments along the 30 m belt transect.

Four measurements were recorded for each plant to model

production. The major axis referred to the longest horizontal

line between living plant tissue across the plant crown. The

minor axis was a similar line perpendicular to the major

axis. Two additional axes were measured perpendicular to

one another and set at 45° angles to the intersection of the

major and minor axes. The modeled forage production per

plant was multiplied by the density of large plants to

determine the mass of sagebrush forage available on a per ha

basis.

Each of the 20 plants measured for production (10 plants x

2 transects) was cut at the base and transported to the lab for

aging (total of 660 large plants). Twenty small immature

plants (<22 cm across the widest portion of their crown) were

collected in the same manner for aging at each of the 33 sites

(total of 660 small plants). Twenty dead plants per site were

also collected, but because dead plants were uncommon and

often not found near the 3 m marks, these plants were

collected by walking through the site and cutting the first 20

plants encountered. Often, dead stems were rotted or colonized by ants and had to be discarded, thus, on some sites,

it was not possible to collect 20 specimens.

Annual growth rings were counted in cross-sections

(Ferguson 1964; Taha 1972). Sagebrush cross-sections were

sanded smooth and a fresh razor was used to take a thin

veneer off the surface. This removed the surface pores that

were filled with sawdust or impurities and clarified the

annual growth rings. A light coating of vegetable oil was

sometimes used to highlight rings before counting with a 10x

hand lens under a full spectrum light.

Results and Discussion __________

The age distribution of large mountain big sagebrush is

shown in figure 2. Ages of individual large plants ranged

from 5 to 88 years with an average age of 32 years. Because

no large plants were less than 5 years old, it appears that 5

years are required for a mountain big sagebrush plant to

reach an age where it is large enough to have a crown >22 cm

at the widest portion. Roughton (1972) excluded all plants

less than 9 years old in his discussion of sagebrush age

classes. When mountain big sagebrush is burned, recovery

to pre-burn levels of forage production is a slow process and

requires almost a decade for shrubs to attain any notable

level of production (Roughton 1972). Further, frequent burning of sagebrush should be expected to reduce sagebrush

forage production (Watts and Wambolt 1996).

The population of sagebrush in the study area is relatively

young. The age classes with the largest number of individual

plants were between 25 and 35 years old. When plants were

grouped as stands (20 plants measured per stand), the

average stand age (n = 33) ranged from 18 to 45 years with

an average overall stand age of 32 years in 1993 (table 1).

Therefore, the average stand age was identical to the average individual age. Only 12 percent of the individuals exceeded 50 years of age, and 5 percent were older than 60

years.

While big sagebrush have been reported to live as long as

200 years (Ferguson 1964), the oldest plant we recorded was

a dead individual of 109 years. The oldest living plant was 88

years of age. In areas such as southwest Montana and

southern Idaho where most sagebrush stands have been

treated in various manners in attempts to improve livestock

forage, the majority of mountain big sagebrush have been

aged at 11 to 20 years with the next most common age class

21 to 30 years (Brown 1982). Although the length of time

since the last disturbance (such as fire) was not discussed,

Brown (1982) found only 3 percent of plants were older than

50 years. In Nevada, the average longevity of big sagebrush

(subspecies not considered) was estimated at 30 to 40 years

(Wallace and Romney 1972). The oldest big sagebrush plant

(subspecies not considered) observed by Roughton (1972) in

Colorado was 72 years old. On two sites, he found that 60 to

75 percent of shrubs were between 5 and 35 years of age (the

0 to 4 year age class was excluded). By excluding age classes

below 9 years, he found that the majority of sagebrush on a

third site was between 50 and 59 years old. He described this

age structure as “decadent” even though thousands more

0

10

20

30

40

50

60

70

80

90

100

0-4 4-9 10-14 15-19 20-24 25-29 30-34 35-39 40-44 45-49 50-54 55-59 60-64 65+

Age class (years)

Number of large plants

Figure 2—Age distribution of 660 large (>22 cm

across widest portion of crown) mountain big sagebrush plants from 33 sites in 1993.

Table 1—Averages and ranges of plant characteristics for 33 mountain

big sagebrush sites.

Standard

Mean deviation Maximum Minimum

Percent live line cover 14.2 0.1 38.8 3.0

Percent dead line cover 5.5 0.0 15.0 0.1

Density large plants/m2 0.9 0.3 1.5 0.4

Density small plants/m2 1.0 1.0 4.0 0.1

Density dead plants/m2 0.2 0.1 0.7 0.1

Winter forage (g/plant) 127.6 73.6 330.1 34.8

Percent deadcrown 22.5 7.2 43.2 11.1

Age large stand 32.2 6.4 45.0 18.0

Age small stand 6.1 0.5 25.0 1.0

Age dead stand 40.7 7.5 56.0 20.0
USDA Forest Service Proceedings RMRS-P-21. 2001 333

Mountain Big Sagebrush Age Distribution and Relationships on the Northern Yellowstone Winter Range Wambolt and Hoffman

plants were observed between 1 and 9 years old than all the

other age classes put together. This description seems misleading because thousands of young replacement plants

were not considered. Although the sagebrush stands apparently had begun a cycle of self-rejuvenation as described by

Lommasson (1948), stands were described by Roughton

(1972) as if the young members were of no consequence.

In the Gardiner Basin of the NYWR, every site measured

had young age classes well represented with the majority of

plants less than 50 years old. Because none of the 33 sites

have been drastically disturbed (as with fire, spraying, and

so forth), this relatively young condition has maintained

itself, with sagebrush plants establishing, maturing, dying

and being replaced in a relatively short period of time

(around 50 years) in the absence of human intervention as

expected from a climax dominant. This indicates that burning or other disturbances are not necessary to maintain

sagebrush stands in a productive state.

Dead mountain big sagebrush plants also provided evidence that mountain big sagebrush stands turn over relatively rapidly without intervention. The average age of dead

plants was 40.7 years (table 1). This does not precisely

establish the age at which mountain big sagebrush are likely

to die because plants with rot were excluded from the

sample. However, the estimate comes from 440 observations, which indicates that turnover by age 41 is not uncommon. Lommasson (1948) reported 40 years as the stand age

at which old mountain big sagebrush plants begin to senesce,

thereby breaking down and creating natural openings in

which young plants may establish. Recruitment by seedlings in closed stands of mountain big sagebrush occurs only

infrequently due to intraspecies competition (Meyer 1994).

However, patterns of seedling establishment are not always

clearly related to natural openings associated with aging

stands. They may also be influenced by environmental

factors such as soil moisture or seed production (Tyrrell and

Crow 1994).

The year of establishment for small mountain big sagebrush individuals is shown in figure 3. Such small plants do

not contribute notably to the production by mountain big

sagebrush in the study area. Occasionally plants that were

over 20 years old and still small were found in areas with

adverse growing conditions such as very dry, shallow soils on

exposed ridgetops.

Individual small mountain big sagebrush plants ranged

from 1 to 25 years old. Nearly one-half of 660 small plants

sampled were 5 years old (germinated in 1988) when sampled

in 1993. This age dominated on all 33 sites. When small

plants were grouped as stands (20 plants per stand), the

average age (n = 33) ranged from 4 to 11 years with an overall

average age of 6 years (table 1).

Crisp and Lange (1976) proposed a model for age structure

of shrubs that under hypothetical natural conditions, mortality is highest in young and old individuals, with reduced

mortality in mature, but relatively young plants. A sharp

decline would occur early after germination, followed by a

period of reduced mortality. Eventually, mortality rates

would again increase after plants reached a critical age.

The average stand establishment dates of large and

small mountain big sagebrush plants are shown in figure 4.

Data were collected from different populations and should

not be combined to form a continuous age structure. The

survivorship curve (fig. 4) from this study area is quite

different from the hypothetical change described in Crisp

and Lange (1976). Within the age distribution for large

plants, several stands have average ages that date to the

late 1940s and early 1950s. Stand ages do not pre-date the

1940s because, as a whole, mountain big sagebrush in this

area were found to average 41 years (table 1). The stands

at the older end of the curve are probably approaching the

lifespan of mountain big sagebrush. This lifespan is influenced in part by the large ungulate populations that have

been present since these plants germinated.

In the late 1950s and early 1960s, mountain big sagebrush

establishment generally increased, reaching a peak in 1961

(fig. 4). This event was followed by a general decrease in

recruitment by the late 1960s. This is inconsistent with the

hypothesis that decreased mortality is observed in mature

301

0

10

20

30

40

50

60

70

80

78 79 80 81 82 83 84 85 86 87 88 89 90 91 92

Year of establishment

Number of small plants

Figure 3—Year of establishment for 660 small (<22 cm

across widest portion of crown) mountain big sagebrush plants from 33 sites.

Figure 4—Large (>22 cm across widest portion of crown)

and small (<22 cm) mountain big sagebrush stands average establishment date and elk winter counts on the

Northern Yellowstone Winter Range.

0

2

4

6

8

10

12

14

16

18

20

1930

1935

1940

1945

1950

1955

1960

1965

1970

1975

1980

1985

1990

Elk Population (thousands)

0

2

4

6

8

10

12

14

16

18

20

Number of Sagebrush Stands

Elk Number

Large Plants

Small Plants

( Poor Count) --
334 USDA Forest Service Proceedings RMRS-P-21. 2001

Wambolt and Hoffman Mountain Big Sagebrush Age Distribution and Relationships on the Northern Yellowstone Winter Range

but relatively young plants (Crisp and Lange 1976). Assuming that plants germinate and establish equally each year

and that survival followed the hypothetical curve described

by Crisp and Lange (1976), then many more site ages should

have been observed in the late 1960s and early 1970s.

However, by the 1970s, establishment of mountain big sagebrush is extremely low.

According to the hypothetical age distribution model (Crisp

and Lange 1976), small mountain big sagebrush should

have high mortality rates that perhaps slow as the plants get

older and begin to mature. Because nearly half of the small

plants measured were 5 years old, their distribution also

contrasts with the hypothetical model. Establishment peaks

dramatically in 1988. This type of establishment was not

found during other years.

The bimodal curve of the age distribution of mountain big

sagebrush corresponds to two distinct reduction events for

the Yellowstone elk population (Tom Lemke, unpublished

report, Montana Fish, Wildlife & Parks, Houston 1982).

Removals of 6,365 animals in the winter of 1955 and 1956

(mostly from outside YNP) and of 5,135 (mostly from

within YNP) in the winter of 1961 to 1962, primarily by

shooting, cut the elk population approximately in half each

year (Houston 1982). During the winter of 1988 and 1989,

snow conditions, coupled with habitat loss from the large

Yellowstone fires the previous summer, resulted in approximately a 40 percent loss of the herd (Tom Lemke, unpublished report, Montana Fish, Wildlife & Parks).

Declines in the elk herd that occurred during these two

periods of sagebrush establishment may partially explain

the difference between the curves in this study and the

hypothetical curve. A reduction in herbivory and trampling

may have increased establishment and survival of mountain

big sagebrush, while declines occurred when elk populations

were high.

Episodic germination due to other environmental conditions may also play a role in determining the age distribution

observed in this study. Daubenmire (1975) found that in

basin big sagebrush (Artemisia tridentata Nutt ssp. tridentata), recruitment of seedlings may be delayed for years until

favorable moisture conditions occur for germination and

establishment. Humphrey (1984) found similar results, although big sagebrush subspecies was not considered.

Microtopographic characteristics of the seedbed and precipitation timing are critical for germination of mountain big

sagebrush (Booth and others 1990; Young and others 1990).

Successful emergence of mountain big sagebrush seedlings

may depend on the amount and timing of spring snowpack

(Meyer 1994). In addition, weather conditions, especially

early drought are the primary factors in causing seedling

mortality (Meyer 1994), although seedlings may be able to

withstand water shortages by early summer (Booth and

others 1990).

Temperature and precipitation records from the years

1977 to 1992 show unusual climatic conditions that may

have contributed to the large number of plants that germinated in 1988 (table 2). The late summer of 1987 was one of

the wettest in the 15 year interval. This moisture corresponded with a period of mountain big sagebrush flowering

and seed production. An increase in water availability during late summer has been shown to increase the growth of

reproductive tissues of big sagebrush (Evans and Black

Table 2—Precipitation extremes during the 15 year

period between 1977 and 1992.

Month Precipitation 15 year ranking

mm

1987

July 910 Wettest

August 410 4th wettest

1988

April 490 2nd wettest

May 920 Wettest

June 120 Driest

July 240 3rd driest

August 36 Driest

1993). The spring of 1988 was also one of the wettest of the

15 years sampled, but was followed by a drought in the

summer and fall. A moist spring would promote seed germination of many plant species, but a summer drought would

likely hamper growth of competing plants. Mountain big

sagebrush, which is drought tolerant relatively soon after

emergence (Booth and others 1990), would likely have higher

survival rates.

The age structure of large and small plants includes two

major episodes of establishment. The event in the late 1950s

and early 1960s may be accounted for in part by the dramatic

declines in the elk population. Detailed climatic conditions

for this period were not found. In 1988, unusual climatic

conditions coupled with an approximately 40 percent reduction in the Yellowstone elk herd may have created an ideal

situation for mountain big sagebrush establishment.

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336 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Sherel Goodrich is Ecologist, Ashley National Forest, Vernal, UT 84078.

Allen Huber is Rangeland Manager, Duchesne Ranger District, Ashley

National Forest, Duchesne, UT 84021.

Abstract —The Bishop Conglomerate forms broad, gently sloping

pediments that include a mantle or veneer of coarse gravel and some

cobble over underlying formations. These pediments cover large

areas at the margins of the Uinta Mountains. Mountain big sagebrush (Artemisia tridentata var. pauciflora) communities cover

rather large areas at the outer edge or lower end of these pedimentplains. These communities are a conspicuous feature of the Diamond Mountain, Brush Creek Mountain, and Taylor Mountain

areas toward the eastern end of the Uinta Mountains.

Consistency, frequency, crown cover, and other features of plants

on these pediment-plains suggest an ecological unit in which biotic

and abiotic components are important to classification.

Features of classification include geomorphology, geology, gradient, soils, vegetation, wildlife, and human values. Classification,

capabilities, values, and management implications are discussed.

Mountain big sagebrush communities are compared to Wyoming big

sagebrush (A. tridentata var. wyomingensis) communities of pediments associated with the Green River. Importance of recognizing

differences between communities of these two sagebrush taxa are

emphasized.

Study Sites and Methods _________

Numerous studies have been established on plateaus of

Bishop Conglomerate of the eastern Uinta Mountains on the

Ashley National Forest. Some of these are listed in table 1.

These and other studies referred to in the following discussion are on file at the Supervisor’s Office of the Ashley

National Forest, Vernal, Utah.

Studies at sites listed in table 1 include Rooted Nested

Frequency and Line Intercept of crown cover of shrubs in

which 500 ft of intercept per site was standard. Studies also

include ground cover determination by a point method.

Procedures for these study methods are described by USDA

Forest Service (1993). Rooted Nested Frequency studies

provide quadrat frequency as well as nested frequency of plant

taxa by which diversity of plant communities can be evaluated.

For this paper quadrat frequency rather than nested frequency

is used to express diversity. Frequency studies at each site

included 100 quadrats of 2.7 ft2

 (50 x 50 cm). The procedures

outlined by USDA Forest Service (1993) for Line Intercept

Mountain Big Sagebrush Communities on

the Bishop Conglomerate in the Eastern

Uinta Mountains

Sherel Goodrich

Allen Huber

specifies including openings in crowns of individual shrubs

as crown cover. Thus the measurements of crown cover

referred to in this paper tend to overrate actual crown cover.

In addition to the above studies, line intercept of crown

cover of shrubs has been measured at 36 other sites in this

ecological unit. In addition production (air dry weight) by

species has been measured at numerous sites of which data

from 31 sites was reviewed for this paper. Production measurements were made by clipping and weighing green weight

of annual growth by individual taxa. For the most part

production measurements were taken from 30 plots of 0.98

ft square for each site. Dry weight was determined from dry

weight tables or by comparing green weight with air dry

weight after air-drying samples in paper bags. Study sites

have a varied history of fire, herbicide applications, livestock

grazing, and other management practices.

Comparisons with Wyoming big sagebrush/grass communities of pediments associated with the Green River are

based on information provided for those communities by

Goodrich and others (1999).

Plant nomenclature follows that of Welsh and others

(1993). Authors of plant taxa are not listed in this paper.

They can be found in Welsh and others (1993).

Abiotic and Biotic Features _______

The Bishop Conglomerate Formation varies from boulderconglomerate to pebble-conglomerate. Deposition of the formation apparently began in Oligocene, or perhaps late

Eocene. It mantles a smooth erosion surface and forms a

pediplain (Winkler 1970). This formation is quite extensive

on the south slope and on the north slope of the Uinta

Mountains. Gradient of the plateau lands of this pediment is

mostly less than 5 percent

At the eastern end of the south slope of the Uinta Mountains, lodgepole pine forests cover upper elevations of this

pediment formation. At mid elevations of the formation,

aspen is common and locally dominant. Toward the lower or

southern edge of the formation, mountain big sagebrushgrass communities are extensive. These sagebrush communities that are below the aspen and lodgepole pine belts are

the focus of this paper.

The study area is included in the Uinta Mountains Section

of the National Hierarchical Framework of Ecological Units

as discussed by McNab and Avers (1994). Consistent with

that framework of ecological units, the study area is classified in this paper at the landtype level as a “Bishop Conglomerate Plateau/Mountain Big Sagebrush Ecological Unit.”

This name reflects abiotic and biotic components of the unit.
USDA Forest Service Proceedings RMRS-P-21. 2001 337

Mountain Big Sagebrush Communities on the Bishop Conglomerate in the Eastern Uinta Mountains Goodrich and Huber

Average annual precipitation for this ecological unit likely

varies between 12 and 20 inches. Frost-free period is 40 to 80

days (Ashcroft and others 1992). Summer thundershowers

are common. Snow depth near the end of winter varies from

about 1 ft in rare or occasional winters to 2 to 3 ft in most

winters. Snow commonly covers the ground from November

through April and through much of May in some years.

Soils are generally Typic or Pachic Argiborolls, Cryoborolls,

and Calciborolls. Calciborolls are likely more common toward

the edges of the formation where the mantle of Bishop

Conglomerate thins and contacts more calcareous substrates.

Soils are generally fine, loamy mixed, fine mixed, or loamyskeletal mixed.

Vascular plant communities are highly diverse with shrubs,

graminoids, and forbs usually well represented (tables 2, 3,

and 4). These communities generally support from 3 to 6 shrub

species, 10 to 12 graminoid species, and 30 to 44 forb taxa.

With a sample size of 100 quadrats of 2.7 ft2 (50 x 50 cm) each,

Table 1—Study sites with nested frequency data.

Study site name Study no. Comments

Taylor Mtn. Exclosure 31–4 Inside an exclosure with fence high enough to exclude wild

ungulates as well as livestock. The exclosure was

constructed in 1962. Data for this paper was taken in 1991.

Taylor Mtn. 31–4D Outside the Taylor Mountain Exclosure with a history of cattle

grazing since before establishment of the Ashley National

Forest in 1908. Rest rotation grazing since 1960 with stocking

rates at about 3.3 acres/AUM*.

Mud Spring 31–-35A Grazing history same as for 31–4D.

Grasshopper 32–66 Cattle grazing since before establishment of the Ashley

National Forest in 1908. Rest rotation and deferred rotation

grazing since 1967 with permitted stocking rates at about

2.74 acres/AUM*

Counting Corral 32–67 Grazing history same as for 32–66.

Diamond 3 32–78 Grazing history same as for 32–66. This site was burned in

1993. Data was taken in 1995 only two years after burning.

*AUM or Animal Unit Month is considered here to be equivalent to the grazing of 1 mature cow with calf for one month.

Table 2—Percent quadrat frequency, average quadrat frequency (Ave. QF), and percent site consistency (percent con.) of plant taxa.

Study sites

Plant taxa 32–66 32–67 31–35A 32–78 31–4 31–4D Average QF Percent con.

Shrubs

Artemisia tridentata pauciflora 41 44 12 3 29 35 27 100

Cercocarpus montanus 1 0 17

Chrysothamnus viscidiflorus 16 2 3 6 10 4 7 100

Eriogonum corymbosum 15 3 17

Mahonia repens 5 1 17

Purshia tridentata 4 47 27 13 50

Symphoricarpos oreophilus 1 8 4 2 10 5 5 100

Graminoids (Poaceae)

Bouteloua gracilis 1 0 17

Bromus anomalus 1 1 1 1 50

Bromus tectorum 1 0 17

Danthonia intermedia 2 0 17

Elymus elymoides 50 66 51 53 25 41 48 100

Elymus lanceolatus 59 81 7 39 39 62 48 100

Elymus spicatus 7 44 1 9 50

Elymus trachycaulus 2 0 17

Festuca ovina 6 47 2 3 9 11 83

Koeleria macrantha 34 1 7 2 6 6 9 100

Poa fendleriana 77 78 21 36 71 54 56 100

Poa pratensis 4 5 6 5 20 7 83

Poa secunda 49 62 28 66 6 1 35 100

Stipa comata 46 18 100 38 11 15 38 100

Stipa hymenoides 1 0 17

Stipa lettermanii 9 34 6 4 20 24 16 100

Stipa nelsonii 9 34 6 4 20 24 16 100

(con.)
338 USDA Forest Service Proceedings RMRS-P-21. 2001

Goodrich and Huber Mountain Big Sagebrush Communities on the Bishop Conglomerate in the Eastern Uinta Mountains

Graminoids (Cyperaceae)

Carex obtusata 5 1 17

Carex petasata 5 1 17

Carex rossii 44 70 34 1 25 67

Perennial forbs

Achillea millefolium 1 6 1 2 2 67

Agoseris glauca 21 3 17 15 9 67

Antennaria microphylla 62 71 4 16 3 25 30 100

Arabis drummondii 3 6 2 33

Arabis holboellii 7 3 2 33

Arabis perennans 1 0 17

Arabis spp. 5 12 7 4 50

Arenaria congesta 94 88 81 85 1 54 67 100

Aster chilensis 1 24 3 5 50

Astragalus agrestis 3 1 17

Astragalus argophyllus 12 14 2 5 50

Astragalus convallarius 21 12 1 11 3 8 83

Astragalus spatulatus 4 1 17

Astragalus tenellus 2 0 17

Balsamorhiza hookeri 85 30 4 89 40 37 48 100

Castilleja lineariifolia 3 17 8 4 50

Cirsium spp. 1 0 17

Comandra umbellata 2 0 17

Crepis acuminata 2 7 2 33

Cryptantha flavoculata 2 0 17

Cymopterus longipes 12 2 17

Delphinium nuttallianum 12 82 1 16 50

Erigeron eatonii 23 42 12 14 15 67

Erigeron flagellaris 12 57 1 33 21 21 83

Erigeron pumilis 7 1 17

Eriogonum umbellatum 1 15 2 26 28 12 83

Gilia aggregata 4 2 2 1 50

Heterotheca villosa 1 4 1 33

Hymenoxys acaulis 2 2 1 33

Lesquerella spp. 2 0 17

Lewisia pygmaea 4 1 17

Linum lewisii 1 0 17

Lithophragma glabra 63 11 17

Lithospermum ruderale 1 1 0 33

Lomatium spp. 9 2 17

Lomatium triternatum 27 2 48 6 11 16 83

Lupinus argenteus 94 77 19 3 35 38 83

Lychnis drummondii 3 1 7 2 50

Mertensia fusiformis 8 5 25 12 4 4 10 100

Penstemon humilis 12 8 5 19 7 67

Penstemon spp. 5 1 17

Petradoria pumila 19 26 8 20 29 17 83

Phlox hoodii 17 3 17

Phlox longifolia 2 39 11 25 13 67

Phlox multiflora 73 4 40 2 16 12 25 100

Potentilla gracilis 14 22 53 16 18 67

Ranunculus glabberrimus 7 1 17

Sedum lanceolatum 31 21 9 33

Senecio integerrimus 43 5 5 17 12 67

Senecio multilobatus 1 1 0 33

Stellaria jamesiana 30 5 17

Taraxacum officinale 3 49 41 3 1 14 19 100

Thlaspi montanum 40 13 9 33

Trifolium gymnocarpon 84 53 51 12 12 49 44 100

Viola nuttallii 4 2 1 33

Zigadenus paniculatus 1 6 20 4 2 8 7 100

Annual forbs

Androsace septentrionalis 10 9 3 33

Chenopodium spp. 7 1 17

Collinsia parviflora 67 97 31 33 50

Collomia linearis 71 82 34 31 50

Draba nemorosa 10 2 17

Gayophytum spp. 53 1 9 33

Gymnosteris parvula 3 1 17

Lappula occidentalis 1 0 17

Lepidium densiflorum 3 1 17

Polygonum douglasii 2 49 64 58 29 67

Table 2 (Con.)

Study sites

Plant taxa 32–66 32–67 31–35A 32–78 31–4 31–4D Average QF Percent con.
USDA Forest Service Proceedings RMRS-P-21. 2001 339

Mountain Big Sagebrush Communities on the Bishop Conglomerate in the Eastern Uinta Mountains Goodrich and Huber

average number of vascular plant taxa was 48 per site, and

average number of taxa per quadrat was 11.35 (table 3).

Except for common dandelion (Taraxacum officinale) and

perhaps Kentucky bluegrass (Poa pratensis), plants found at

study plots across the ecological unit are mostly native to the

area. Other introduced plants are of low consistency and of

low frequency. An exception to native plant dominance is

found in areas that have been seeded to smooth brome

(Bromus inermis) and intermediate wheatgrass (Elymus

hispidus).

Vascular plant production (table 5) is generally high

enough to produce a ground cover of vegetation and litter

that covers over 90 percent of the soil surface (table 6). With

this extent of vascular plant and litter cover, cryptogrammic

crusts appear to be of minor importance as ground cover.

Table 3—Vascular plant diversity and ground cover.

Crown cover of

Site Alpha Beta sagebrush Ground cover

- - - - - - - - - Percent - - - - - - - - -

32–66 11.66 40 16.4 95

32–67 11.64 44 15.1 87

32–78 11.20 46 0.2 65a

31–35A 10.91 45 5.0 87

31-4 5.98b 46 32.4c 95

31–4D 14.1 67 — 95

Average 11.35 48 92d

a

At 1.5 growing seasons after fire. Not included in average.

bInside a 30-year old exclosure. Not included in average.

c

In addition to sagebrush cover, crown cover of bitterbrush was 37.9 percent.

Total crown cover of these two shrubs was 70.3 percent. d All sites included in this average have a long history of livestock grazing.

Table 4—Plant taxa with 100 percent site consistency at 6 sites on

Bishop Conglomerate Plateau/Mountain big sagebrush

ecological unit.

Average quadrat*

Taxon Site consistency frequency

- - - - - - - - - - - - n = 6 - - - - - - - - - - - - -

Mountain big sagebrush 100 27

Yellowbrush 100 7

Mountain snowberry 100 5

Squirreltail 100 48

Thickspike wheatgrass 100 48

Muttongrass 100 56

Sandberg bluegrass 100 35

Needle-and-thread grass 100 38

Letterman needlegrass 100 16

Pussytoes 100 30

Ballhead sandwort 100 67

Hooker balsamroot 100 48

Bluebells 100 10

Many-flowered phlox 100 25

Dandelion 100 19

Hollyleaf clover 100 44

Death camas 100 7

*Quadrat size is 19.7 x 19.7 inches (50 x 50 cm).

Table 5—Production (lbs/acre air dry wt.) at

various shrub cover.

Percent shrub cover

0–10 11–20 >20

(n = 17) (n = 8) (n = 6)

Graminoids 637 193 167

Forbs 175 204 179

Shrubs 37 660 915

Total 847 1054 1261

Table 6—Percent of production at various shrub

cover.

Percent shrub cover

0–10 11–20 >20

(n = 17) (n = 8) (n = 6)

Graminoids 75 18 13

Forbs 21 19 14

Shrubs 4 63 73

Total 100 100 100

Vascular Plants and Community

Dynamics ______________________

Plant communities are highly diverse with high numbers

of vascular plants (table 2). Vascular plants of high site

consistency and high quadrat frequency are considered here

to be the most descriptive of the ecological unit. Those with

higher values are listed in table 4, and some of these are

included in the following discussion.

Mountain Big Sagebrush

Crown cover of mountain big sagebrush on this ecological

unit has been found between 0 percent and 38 percent

depending on fire and other processes and management

actions. As mentioned above the method used to determine

crown cover tends to over estimate crown cover. The data

indicate crown cover of sagebrush rarely, if ever, exceeds an

average of 40 percent on sites of over 0.75 acres. Following

fire, herbicide application, and plowing and seeding, sagebrush cover has been decreased to 0 percent. Within 15 to 25

years mountain big sagebrush has returned to pretreatment

crown cover at most sites. At a few sites this happened in as

little as 10 years. At sites plowed and seeded to aggressive

grasses such as smooth brome and intermediate wheatgrass, the return of sagebrush has been slower. In some of

these cases, sagebrush has not returned to pretreatment

status after 40 years. However, it is present and slowly

increasing in most of these treatments.

Essentially all of the dynamics of sagebrush studied or

observed on this landscape has been concurrent with a long

history of livestock grazing. It appears that livestock grazing

has accelerated return of sagebrush after fire and herbicide

applications. It also appears livestock grazing can push
340 USDA Forest Service Proceedings RMRS-P-21. 2001

Goodrich and Huber Mountain Big Sagebrush Communities on the Bishop Conglomerate in the Eastern Uinta Mountains

Other Shrubs

Average number of shrub taxa at nested frequency study

sites was four. Both yellowbrush (Chrysothamnus

viscidiflorus var. lanceolatus) and mountain snowberry

(Symphoricarpos oreophilus) had 100 percent site consistency, but these had rather low quadrat frequency values

(table 2). Yellowbrush and mountain snowberry appear to

play a minor part in driving plant community dynamics.

Although these shrubs sometimes show slight increase in

early postfire years, crown cover of these shrubs rarely

exceeds 2 percent. Other plants appear to be little influenced

by these shrubs. However, bitterbrush is locally common to

abundant on this ecological unit, and at high percent crown

cover it appears to have at least moderate capacity to

suppress other species.

Graminoids

Average number of graminoid taxa was 12 (table 3).

Graminoids with 100 percent site consistency (n = 6) and

with quadrat frequency of greater than 33 percent are

muttongrass (Poa fendleriana), Sandberg bluegrass (P. secunda), needle-and-thread grass (Stipa comata var.

intermedia), thickspike wheatgrass (Elymus lanceolatus),

and squirreltail (E. elymoides). Two other grasses had 100

percent site consistency but had less than 33 percent quadrat frequency. These were Junegrass (Koeleria macrantha)

and Letterman needlegrass (Stipa lettermanii). As indicated

in table 5, graminoids are most productive when sagebrush

canopy cover is less than 10 percent. However, they appear

to be able to persist in sufficient abundance and vigor under

as high as 30 percent crown cover of sagebrush to be able to

rapidly respond to fire that decreases sagebrush cover.

Bluebunch wheatgrass (Elymus spicatus) is lacking or of

low quadrat frequency at most sites. Grazing does not

appear to be the factor in the absence of bluebunch wheatgrass, for it is abundant to dominant on adjacent, warmer

ecological units of the south face of the Uinta Mountains

with equal grazing history. The one site with over 10 percent

quadrat frequency of bluebunch wheatgrass (31-4D) is at the

ecotone with the south face of the Uinta Mountains.

Sheep fescue (Festuca ovina) had 83 percent site consistency, but average quadrat frequency of this plant was only

11 percent. Low frequency of this plant does not seem to be

a function of grazing. More frequent graminoids are used

equally or to a greater degree than is sheep fescue on this

ecological unit. Also the sheep fescue complex is not found in

great abundance in many areas of the Uinta Mountains that

have been quite protected from livestock. Inherent factors

appear to limit plants of this complex here.

Muttongrass appears to be the graminoid most capable of

persisting at moderate to high frequency under high percent

canopy cover of sagebrush. The ability of muttongrass to

persist under dense canopy of sagebrush on this ecological

unit indicates value of this plant as a descriptor of the

sagebrush community type or habitat type for the area.

Needle-and-thread grass appears to be the graminoid most

capable of rapid increase following fire.

Graminoids appear to drive community dynamics in early

successional stages. They dominate production in the early

crown cover of sagebrush beyond levels that would be found

in absence of livestock grazing. However, as noted by Knight

(1994) for Wyoming, presence of sagebrush should not be

considered an artifact of livestock grazing. The conclusion of

Johnson (1984) that the current distribution of sagebrush

matches the distribution prior to settlement seems highly

applicable to this ecological unit. Livestock grazing appears

to have done little to move sagebrush beyond its presettlement

distribution. It appears livestock grazing can increase sagebrush cover in areas were it existed prior to settlement. This

is more likely for persistent, heavy use by livestock than for

light or moderate use.

Snow mold and other features of winter can damage

sagebrush (Nelson and Tiernan 1983; Sturges and Nelson

1986). Winter damage of sagebrush is evident on parts of

this ecological unit. This is more conspicuous on concave and

flat topography than on convex topography. At one study site

(32-66), crown cover of sagebrush was decreased from 16

percent down to 5 percent in 7 years. At some other sites

winter damage has limited sagebrush crown cover to less

than 10 percent over as many as 4 decades (site 32-14). Other

agents of injury to sagebrush include rodents that girdle the

stems (Frischknecht and Baker 1972; Sturges 1983).

Regardless of agents of injury and mortality, including

fire, herbicide applications, rodents, insects, and winter

damage, mountain big sagebrush has persisted as a landscape dominant on the study area for several decades and

probably thousands of years. Although livestock are likely to

have increased crown cover of sagebrush on this area, the

competitive ability of sagebrush indicates it was a strong

component of these communities prior to introduction of

Euro-American livestock.

With high ability to return after disturbance, sagebrush is

clearly a major force in plant community dynamics. Other

plant species generally respond or react to sagebrush. This

is demonstrated in response of the understory to sagebrush

reduction and recovery. As shown in tables 5 and 6, graminoid

production is highly sensitive to crown cover of sagebrush.

At 0 to 10 percent crown cover of sagebrush, graminoids

produced an average of 637 lbs/acre (air dry weight) or 75

percent of annual herbage production. At 20 to 30 percent

crown cover of sagebrush, graminoid production was decreased to an average of 167 lbs/acre or 13 percent of total

production. Forbs respond similarly to grasses. However,

the range of variation is narrower. At 0 to 10 percent crown

cover, sagebrush contributed 4 of production. At 20-30 percent crown cover it increased to 73 percent of production.

The influence of high percent crown cover of shrubs is

also indicated in alpha diversity as shown in table 3 for site

31-4. Crown cover of shrubs at that site far exceeded that of

other sites, and alpha diversity was only about 1

⁄

2 as high as

at other sites.

Regardless of high percent crown cover of sagebrush and

its suppression of the understory, the understory of this area

appears to have high capacity to increase rapidly after

disturbances that decrease sagebrush. As many as 37 forbs,

12 graminoids, and 4 shrubs have been found on burned sites

at 2 years postfire. Plant and litter cover have been found as

high as 90 percent at 5 to 7 years following fire (study sites

32-70 and 32-78), and this was concurrent with livestock

grazing.
USDA Forest Service Proceedings RMRS-P-21. 2001 341

Mountain Big Sagebrush Communities on the Bishop Conglomerate in the Eastern Uinta Mountains Goodrich and Huber

years following fire and following herbicide application.

However, they appear to be highly compatible with high

diversity of forbs in the early years following disturbance.

Forbs

As high as 37 forb taxa have been recorded for a site with

sample size of 100 quadrats of 2.7 ft2

. Average number of

forb taxa was 31 (table 7). Those with 100 percent site

consistency and greater than 33 percent quadrat frequency

(table 2) are ballhead sandwort (Arenaria congesta), Hooker

balsamroot (Balsamorhiza hookeri), and hollyleaf clover

(Trifolium gymnocarpon). Others with 100 percent site consistency but with less than 33 percent quadrat frequency are

pussytoes (Antennaria microphylla), bluebells (Mertensia

fusiformis), many-flowered phlox (Phlox multiflora), common dandelion, and death camas (Zigadenus paniculatus).

Of these forbs ballhead sandwort, hollyleaf clover manyflowered phlox, and hooker balsamroot seem to be of some

importance to classification of this ecological unit. By

themselves they are not unique to this ecological unit, for

they are widely distributed. However, collectively they

appear to be quite descriptive of the unit. This ecological

unit appears to be the principal habitat for many-flowered

phlox in Utah.

Forbs appear to react to community dynamics more than

to drive these dynamics. They decrease or increase in reaction to shrub and graminoid changes. Some, including ball

head sandwort, dandelion, and pussytoes might be expected

to increase with increasing intensity of ungulate grazing.

Fire

References that indicate fire of rather high frequency

burned in communities of this ecological unit include Houston (1973) and Winward (1991). Additional evidence of

comparatively high fire frequency includes the volatile nature of mountain big sagebrush communities. Based on a

large number of prescribed fires and attempted prescribed

fires on the Ashley National Forest, basin big sagebrush and

mountain big sagebrush communities are among the most

easily ignited communities with capability to carry fire

under weather conditions that will not support fire in many

other plant communities.

The capability of sagebrush/grass communities to carry

wildfire was well demonstrated in the Dry Fork Fire of 2000

on the south slope of the Uinta Mountains. In this fire, a

sagebrush/grass community of the south face of the Uinta

Mountains was the ignition source. From that point the fire

was carried onto sagebrush communities of the Bishop

Conglomerate Formation. These communities carried the

fire into aspen and lodgepole pine communities.

Fire adapted species that occupy plant communities of

this ecological unit are additional evidence of high fire

frequency. As high as 37 forb taxa, 12 graminoid taxa, and

4 shrub taxa have been found in burned areas at two growing

seasons postfire (site 32-78). Plants found in postfire communities are the same ones found prior to burning. Fire

alters abundance of various taxa in different ways, but it

seems to do little to change the presence of taxa.

Although sagebrush is greatly reduced by fire, it is not

uncommon to find seedlings of sagebrush the year after fire.

Indeed the dynamics of mountain big sagebrush itself is a

strong indication of high adaptability to fire. It is common for

mountain big sagebrush to return to 20 percent canopy cover

within 15 to 25 years after fire. The recovery interval of

sagebrush of 15 to 25 years could, perhaps, be an indicator

of the fire return interval common to the history of this

ecological unit.

Postfire response of bitterbrush appears to be more varied

than for sagebrush. It generally increases after the initial

reduction following fire, but recovery is much slower on some

sites than on others.

Some other species increase rapidly in the first 1 to 3 years

following fire including annuals such as blue-eyed Mary

(Collinsia parviflora) and ground smoke (Gayophytumspp.).

Abundance of these appears to be fire-dependant, as these

Table 7—Comparison of features of Wyoming big sagebrush communities (ARTRW) from

pediments associated with the Green River and mountain big sagebrush communities

(ARTRP) on the Bishop Conglomerate Plateau.

Community feature ARTRW (n = 9) ARTRP (n = 6*)

Crown cover of sagebrush (percent) 0–22 0–38

Total number of vascular plant taxa 51 93

Total number of shrub taxa 7 7

Total number of graminoid taxa 13 20

Total number of forb taxa 26 66

Ave. number taxa/site (alpha diversity) 18 47

Ave. number of taxa/quadrat (beta diversity) 2.92 11.35

Ave. number of shrub taxa/site 4 4

Ave. number of graminoid taxa/site 6 12

Ave. number of forb taxa/site 7 31‘

Shrubs with 100 percent consistency 1 3

Shrubs with >49 percent consistency 1 4

Graminoids with 100 percent consistency 1 7

Graminoids with >49 percent consistency 7 12

Forbs with 100 percent site consistency 0 8

Forbs with >49 percent site consistency 4 31

Average ground cover (percent) 58 92

*n = 6 except for crown cover of sagebrush for which n = 42.
342 USDA Forest Service Proceedings RMRS-P-21. 2001

Goodrich and Huber Mountain Big Sagebrush Communities on the Bishop Conglomerate in the Eastern Uinta Mountains

species seem to respond from a soil-seedbank of long-lived

seeds that are activated by fire. Regardless of the initial

response to fire, nearly all species of the ecological unit show

adaptability to fire. They increase after fire by soil-seedbanks, by sprouting, or by mobile seeds that are produced

elsewhere but are transported to burned areas.

Capabilities and Values __________

Due to low gradient, the pediment surface, and capacity to

produce 90 percent or more ground cover, this ecological unit

is resistant to erosion. Roads across the unit are comparatively stable. This ecological unit has supported livestock

grazing for about a century with little evidence of accelerated erosion.

Vascular plant diversity and ground cover have been

maintained at high levels concurrent with livestock grazing.

These features indicate this area has moderate to high

capability to support livestock grazing concurrent with

maintenance of a number of other values.

McArthur (1984) reported 87 wildlife species for sagebrush communities of the Intermountain Region. While

total number of wildlife species can be expected to be less

than this on any one ecological unit, high diversity of wildlife

species are indicated for this one by the high diversity of

plant communities of the unit. It has high capability to

produce high value herbaceous forage and browse for wild

ungulates.

Bitterbrush is closely hedged across the unit. This indicates high value of this plant for ungulates. However, mountain big sagebrush is lightly, if at all, hedged over much of

the area. Hedging of this shrub by ungulates seems to be

more prominent toward the lower edges of the unit where it

contacts the south face of the Uinta Mountains where wild

ungulates spend more time in winter.

This ecological unit has capability to support dense stands

of sagebrush of high value for sage grouse nesting. High

number of forbs and relative high production of forbs indicate high value brooding habitat for sage grouse. The unit

also includes mesic drainages that support graminoid and

forb dominated communities of high value for sage grouse

brooding. Current numbers of sage grouse are much lower

than in past decades. Livestock grazing was equally intense

or of greater intensity in past decades than in the past few

years. The history of sage grouse populations and the history

of livestock grazing indicate factors other than livestock

grazing are related to declines in sage grouse populations.

Compared to forested environments, wild ungulates are

highly visible in the sagebrush communities of this ecological unit. Wild ungulates are abundantly seen on the unit in

spring and mild winters. This indicates high value for

recreational wildlife viewing. The high capacity of this unit

to support wild ungulates also translates to high value for

big game hunting opportunities.

Camping associated with this ecological unit is most

common at its margin with the aspen and lodgepole pine

ecotone. However, the unit does have low to moderate value

for camping.

As discussed above, the ecological unit is highly capable of

supporting fire and recovering from fires with frequency of

25 to 40 years.

Comparison of Mountain Big

Sagebrush Communities With

Wyoming Big Sagebrush

Communities ___________________

Goodrich and others (1999) reported on Wyoming big

sagebrush/grass communities of pediments associated with

the Green River in Daggett County, Utah. These communities are at the base of the north flank of the Uinta Mountains

where average annual precipitation is about 9 inches and

snow depth is commonly less than 1 foot, and continuous

snow cover is usually limited to December through February. In that environment crown cover of sagebrush was

found from 0 to 22 percent compared to 0 to 38 percent in

mountain big sagebrush communities of plateau lands of the

Bishop Conglomerate Formation.

Hedging of sagebrush by wild ungulates is heavy in the

Wyoming big sagebrush communities associated with pediments of the Green River. Hedging of sagebrush is light to

locally moderate in the mountain big sagebrush communities

on Bishop Conglomerate. Difference in hedging of sagebrush

is likely a function of differences in snow depth and duration.

Difference in hedging is also a function of pronghorn antelope

(Antilocarpa americana). Pronghorn diets can include high

percent of sagebrush (Cole 1956; Ngugi and others 1992;

Olsen and Hansen 1977). Pronghorn are abundant during

parts of the year in some of the Wyoming big sagebrush

communities. They are rare to lacking in the mountain big

sagebrush communities on Bishop Conglomerate.

While greater hedging of sagebrush by mule deer and

pronghorn is a factor in difference of sagebrush crown cover,

the primary factor is likely the climate and especially precipitation. Nine inches of annual precipitation of the Wyoming big sagebrush communities does not have the capacity

to support as much sagebrush cover as does 12 to 20 inches

of the mountain big sagebrush communities. This concept is

supported by exclosures in the Wyoming big sagebrush

communities that have prevented ungulate access. In these

exclosures, sagebrush has not exceeded an average of 22

percent crown cover (Goodrich and others 1999). Other

differences between communities of the two sagebrush taxa

discussed below are considered to be primarily a function of

climate.

Ground cover averaged about 55 to 59 percent in areas

protected from livestock or that were grazed at moderate

intensity in Wyoming big sagebrush communities compared

to 90 percent or more ground cover concurrent with moderate to heavy livestock grazing in mountain big sagebrush

communities.

Average number of vascular plant taxa was 19 and 47 for

Wyoming big sagebrush and mountain big sagebrush communities respectively. Perhaps the most vivid contrast is

seen in the number of forb taxa and production of forbs.

Average number of forb taxa was 7 and 31 for Wyoming big

sagebrush and mountain big sagebrush communities respectively (see table 7 for these and other comparisons).

Production (air dry weight) of forbs in mountain big sagebrush communities of the Bishop Conglomerate Plateau

ranged from 25 to 365 lbs/acre depending on the crown cover

of sagebrush. Forb production in Wyoming big sagebrush
USDA Forest Service Proceedings RMRS-P-21. 2001 343

Mountain Big Sagebrush Communities on the Bishop Conglomerate in the Eastern Uinta Mountains Goodrich and Huber

communities of Green River pediments is commonly as low

as 3 to 10 lbs/acre.

Another conspicuous difference is the absence of bitterbrush in Wyoming big sagebrush communities and the

presence and sometimes abundance of bitterbrush in mountain big sagebrush communities. Plants of Chrysothamnus

viscidiflorus are present in communities of both sagebrush

taxa. However, there is a difference at the level of variety.

Sticky rabbitbrush (Chrysothamnus v. var. viscidiflorus) is

specific for Wyoming big sagebrush communities, and

yellowbrush is found at high consistency in mountain big

sagebrush communities. Also mountain snowberry is consistently found in mountain big sagebrush communities of this

ecological unit, but it is lacking in the Wyoming big sagebrush communities along the Green River.

Although needle-and-thread grass was of 100 percent

consistency in both Wyoming big sagebrush and mountain

big sagebrush communities, the long-awned variety (Stipa

comata var. comata) was found only in Wyoming big sagebrush communities, and the short-awned variety (S. c. var.

intermedia) was found only in mountain big sagebrush

communities.

Management Implications ________

Mountain big sagebrush communities of the Bishop Conglomerate Plateau have diverse capabilities and values.

These lands have been managed for multiple uses over the

past several decades concurrent with maintaining ground

cover and highly diverse plant communities. These uses

appear to be compatible with maintaining processes such as

fire and successional patterns consistent with the inherent

capability of the land. The history of use and response to use

indicates these communities have capability to continue to

be managed for a number of uses concurrent with maintaining long-term productivity.

Inherent capabilities of mountain big sagebrush/grass communities of Bishop Conglomerate pediments and Wyoming

big sagebrush/grass communities of pediments associated

with the Green River are vastly different. Values expected of

these communities could be outside reality if these differences

are not recognized. Expectations for Wyoming big sagebrush

communities based on a vision of mountain big sagebrush

communities are indicated for disappointment, and they can

be expected to lead to expensive failures in terms of habitat

improvement projects.

The Wyoming big sagebrush communities have high value

as winter range for mule deer and pronghorn and, in places,

high value year-long for pronghorn. The mountain big sagebrush communities have high value for mule deer in spring,

fall, and mild winters. They have low value for mule deer in

normal and heavy winters, and they have low value for

pronghorn year-long.

While the Wyoming big sagebrush communities might be

of moderate to high value for sage grouse wintering areas,

the low capability of these to produce forbs indicates low

value for brooding habitat. Number of forbs and production

of forbs in the mountain big sagebrush/grass communities of

Bishop Conglomerate indicate high value brooding habitat

for sage grouse.

Rating systems for condition and trend based on diversity,

production, and species composition will not reflect reality

unless the inherent differences between communities of

these two sagebrush taxa are recognized.

References _____________________

Ashcroft, G. L.; Jensen, D. T.; Brown, J. L. 1992. Utah climate.

Logan, UT: Utah State University, Utah Climate Center. 125 p.

Cole, G. F. 1956. The pronghorn antelope its range use and food

habits in central Montana with special reference to alfalfa. Tech.

Bull. 516. Bozeman, MT: Montana State College, Agricultural

Experiment Station. 63 p.

Frischknecht, N. C.; and Baker, M. F. 1972. Voles can improve

sagebrush rangelands. J. Range Manage. 25: 466–468.

Goodrich, S.; Nelson, D.; Gale, N. 1999. Some features of Wyoming

big sagebrush communities on gravel pediments of the Green

River in Daggett County, Utah. In: McArthur, E. D.; Ostler, W. K.;

Wambolt, C. L. comps. 1999. Proceedings: shrubland ecotones;

1998 August 12–14; Ephraim, UT. Proc. RMRS-P-11. Ogden UT:

U.S. Department of Agriculture, Forest Service, Rocky Mountain

Research Station: 159–167.

Houston, D. B. 1973. Wildfires in northern Yellowstone National

Park. Ecology 54: 1111–1117.

Johnson, K. L. 1986. Sagebrush over time: A photographic study of

rangeland change. In: McArthur, E. D.; Welch, B. L. comps.

Proceedings—symposium on the biology of Artemisia and

Chrysothamnus; 1984 July 9–13; Provo, UT. Gen. Tech. Rep. INT200. Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Research Station: 223–232.

Knight, D. H. Mountains and plains: The ecology of Wyoming

landscapes. New Haven, CT: Yale University Press. 338 p.

McArthur, E. D. 1994. Ecology, distribution, and values of sagebrush within the Intermountain Region. In: Monsen, S. B.;

Kitchen, S. G., comps. Proceedings—ecology and management of

annual rangelands; 1992 May 18–21; Boise, ID. Gen. Tech. Rep.

INT-313. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Intermountain Research Station: 347–351.

McNab, W. H.; Avers, P. E. comps. 1994. Ecological subregions of the

United States: Section descriptions. Administrative Publication

WO-WSA-5. Washington, DC: U.S. Department of Agriculture,

Forest Service. 267 p.

Ngugi, K. R.; Powell, J.; Hinds, F. C.; and others. 1992. Range

animal diet composition in southcentral Wyoming. J. Range

Manage. 45: 542–545.

Nelson, D. L.; Tiernan, C. F. 1983. Winter injury of sagebrush and

other wildland shrubs in the western United states. Research

Paper INT-314. Ogden, UT: U.S. Department of Agriculture,

Forest Service, Intermountain Forest and Range Experiment

Station. 17 p.

Olsen, F. W.; Hansen, R. M. 1977. Food relations of wild freeroaming horses to livestock and big game, Red Desert, Wyoming.

J. Range Manage. 30: 17–20.

Sturges, D. L. 1983. Long-term effects of big sagebrush control on

vegetation and soil water. J. Range Mange. 36: 720–765.

Sturges, D. L.; Nelson, D. L. 1986. Snow depth and incidence of

snowmold disease on mountain big sagebrush. In: McArthur, E.

D.; Welsh, B. L. comps. Proceedings—Symposium on the biology

of Artemisia and Chrysothamnus; 1984. July 9–13; Provo, UT.

Gen. Tech. Rep. INT-200. Ogden, UT: U.S. Department of

Agriculture, Forest Service, Intermountain Research Station:

215–221.

U.S. Department of Agriculture, Forest Service. 1993. Rangeland

ecosystem analysis and management handbook. FSH 2209.21.

Ogden, UT: U.S. Department of agriculture, Forest Service,

Intermountain Region. Paginated by chapter.

Welsh, S. L.; Atwood, N. D.; Goodrich, S.; Higgins, L. C. 1993. A

Utah flora. Provo, UT: Brigham Young University Print Services. 986 p.

Winkler, G. R. 1970. Sedimentology and geomorphic significance of

the Bishop Conglomerate and the Browns Park Formation, eastern Uinta Mountains, Utah, Colorado, and Wyoming. Salt Lake

City, UT: University of Utah. 115 p. Thesis.

Winward, A. H. 1991. Management in the sagebrush steppe. Special

Report 880. Corvallis, OR: Oregon State University, Agricultural

Experiment Station. 7 p.
344 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Sherel Goodrich is an Ecologist, Ashley National Forest, U.S. Department

of Agriculture, Forest Service, Vernal, UT 84078. Robert M. Thompson is a

Range Conservationist, Manti-LaSal National Forest, U.S. Department of

Agriculture, Price, UT 84501. Allen Huber is a Rangeland Manager, Ashley

National Forest, U.S. Department of Agriculture, Duchesne, UT 84021.

Abstract—Ecological inventory and vegetation monitoring in the

Uinta Mountains and Utah Plateaus on the Ashley National Forest

and Manti-LaSal National Forest of the past several years suggest

a community type in which yellowbrush (Chrysothamnus viscidiflorus ssp. lanceolatus), and slender wheatgrass (Elymus trachycaulus) are indicator species. This community type is common at

elevations or slope positions where snow depth and duration are

sufficient to greatly suppress big sagebrush. Features of this community type are discussed in context of management implications.

Yellowbrush ____________________

Yellowbrush (Chrysothamnus viscidiflorus spp. lanceolatus) is a common plant over much of mid montane Utah.

It is known from lower British Columbia east to Montana

and south to northern California and Colorado with outlying populations in Arizona and New Mexico (Anderson

1986). By association with some of its generic relatives,

yellowbrush has been much maligned. However, yellowbrush

has high value for ungulate forage. In late summer, fall, and

winter it is highly selected by domestic and wild ungulates.

It has been rated with moderate value for watershed protection (USDA Forest Service 1993).

In numerous studies on the Ashley National Forest, it has

not displaced other vegetation by forming dense, closed

stands as is sometimes the case of other members of the

genus. Most often it contributes to species diversity and

structural diversity without assuming high dominance that

greatly suppresses other plant taxa. In contrast to rubber

rabbitbrush (Chrysothamnus nauseosus) and big sagebrush

(Artemisia tridentata), yellowbrush commonly does not overtop associated herbaceous vegetation. It is not uncommon

for associated grasses to exceed the height of yellowbrush.

Even at sites where yellowbrush is a dominant with high

frequency and high percent crown cover, there is usually a

diverse mix of other plant species. Such sites are the focus of

this paper.

The common name of yellowbrush is used in this paper to

reduce association of this plant with some other members of

the genus with less forage value and of more aggressive

A Yellowbrush/Grass Community Type From

the Uinta Mountains and Utah Plateaus

Sherel Goodrich

Robert M. Thompson

Allen Huber

nature. This common name has a long history. It was used

as early as 1937 (USDA Forest Service 1937). Other common

names included mountain low rabbitbrush, lanceleaf yellowbrush, lanceleaf rabbitbrush, and Douglas rabbitbrush.

Study Sites_____________________

Information for this paper came from seven sites on the

Wasatch Plateau, Manti-LaSal National Forest, and from

five sites on the Ashley National Forest. Of the Ashley

National Forest sites, three were from the western Uinta

Mountains, and two were from the West Tavaputs Plateau.

Range in elevation of the sites was from 2,743 to 3,048 m

(9,000 to 10,000 ft). Average elevation of the sites was

2,936 m (9,633 ft). Study sites included all exposures except

northerly. Gradients were mostly from 0 to 15 percent.

Study sites from the Manti-LaSal National Forest are identified as RR-102, YB-1, WH-1, TSR-1, WR-1, CB-101, and

RR-102N. Those from the Ashley National Forest are identified as 34-2, 34-3, 35-5, 58-1B, and 58-2. Locations for these

study sites are documented at the Supervisors Offices of

these National Forests at Price, Utah, and Vernal, Utah.

Methods _______________________

Data was taken from long-term monitoring sites that are

permanently marked and included in study inventories of

the Ashley National Forest and Manti-LaSal National Forest. Plots from which information was taken were of various

sizes and from various methods of vegetation measurements. These included percent composition based on air-dry

weight, rooted nested frequency, and line intercept. Although plot size varied and purpose and design of studies

varied, the plot data does provide site consistency and plot

frequency. Because various plot sizes and various numbers

of plots were used, percent site consistency and percent

frequency is used to standardize the information from the

data.

Although percent composition by weight might not be

statistically friendly, it does provide comparative information. This method of vegetation measurement does provide

a comparative measure of the ability of different plant taxa

to command the resources of a site. Ability to command

resources is perhaps more accurately expressed by relative

production than by frequency. Small annuals of high frequency might be much less able to command resources than

larger plants of lower frequency. Percent composition by

weight (table 1) is one of the parameters used in this paper

to define yellowbrush-grass communities.
USDA Forest Service Proceedings RMRS-P-21. 2001 345

A Yellowbrush/Grass Community Type From the Uinta Mountains and Utah Plateaus Goodrich, Thompson, and Huber

Features of Yellowbrush/Slender

Wheatgrass Communities

Yellowbrush/slender wheatgrass communities are typically found at higher elevations than mountain big sagebrush communities or on concave leeward slopes where

persistent snowbeds suppress sagebrush. They appear to be

more common on basic substrates than on acidic or neutral

ones. In Utah, they are found in the aspen and spruce-fir

belts. They are found in the western Uinta Mountains and on

the plateaus that run down through the center of Utah.

Ground cover (ground covered by vegetation, litter, and rock

greater then 2 cm diameter) varied between 35 and 98

percent with three sites at 35 percent and three sites over

90 percent. Potential for ground cover might be above 90

percent. Sites with lower ground cover values were highly

disturbed by northern pocket gophers (Thomomys talpoides).

Yellowbrush communities are distinguished by yellowbrush being the dominant shrub and sometimes the only

shrub with greater than a trace of crown cover. Line intercept of crown cover of yellowbrush was measured at three of

the sites. Crown cover of this shrub ranged from 8 to 37

percent. Graminoid representatives of these communities

include slender wheatgrass (Elymus trachycaulus), letterman

needlegrass (Stipa lettermanii), and Hood sedge (Carex

hoodii). Although mountain brome (Bromus carinatus) is

occasional to these communities, it is not nearly so common

here as in tall forb communities. Forbs common to these

communities include peavine (Lathyrus lanzwertii), yarrow

(Achillea millefolium), Rydberg penstemon (Penstemon

rydbergii) and Watson penstemon (Penstemon watsonii).

Although yarrow was found at relatively high site consistency, and high plot frequency, this plant is a generalist of

broad ecological amplitude. Its broad amplitude limits the

indicator value of this plant for a specific community type.

The same might be said of Letterman needlegrass.

Several species had site consistency of 33 percent or

greater. However, due to broad amplitude or low plot frequency these plants are not considered reliable or specific

indicators of yellowbrush/grass communities. These include

Sandberg bluegrass (Poa secunda), sedges (Carex spp.),

everywhere aster (Aster chilensis), potentilla (Potentilla

spp. and mostly P. gracilis), dandelion (Taraxacum officinale),

Douglas knotweed (Polygonum douglasii),oniongrass (Melica

bulbosa), rockcress (Arabis spp.), American vetch (Vicia

americana), muttongrass (Poa fendleriana), and penstemon

(Penstemon spp. and mostly P. rydbergii and P. watsonii).

Over 70 vascular plant taxa were recorded in plots. The 17

taxa listed in table 1 had site consistency of 33 percent or

greater. All other taxa had site consistency less than 33

percent, average plot frequency less than 15 percent, and

contributed no more than 1 percent of composition by weight.

The three methods of classifying plants of table 1 all point

to the same few taxa as being most reliable as indicators of the

community type. These are yellowbrush, slender wheatgrass,

Letterman needlegrass, and peavine. The large gap in site

consistency from 92 percent to 58 percent between peavine

and mountain brome shown in table 1 is likely significant.

These plants have rather broad amplitude. However, the

combination of these plants as dominants does seem unique.

The name of yellowbrush/slender wheatgrass serves well to

identify this community type.

Abundance of slender wheatgrass, mountain brome,

peavine, and other plants common to tall forb communities

might be considered an indication that yellowbrush/slender

wheatgrass communities are degraded tall forb communities. However, the classic indicators of degraded tall forb

communities including western cone flower and tar weed

were lacking or of comparatively low frequency at these

sites. Of the 12 sites, tarweed was found at only one site.

Western coneflower (Rudbeckia occidentalis) was not

recorded in plots at any of the sites. Tall larkspur (Delphinium occidentale) was found in low abundance at one site.

Additional evidence of two distinct communities includes

abrupt boundaries between some tall forb and yellowbrush/

slender wheatgrass communities. However, gradual gradients between the two communities can be expected at some

locations.

At the warm or low elevation end, yellowbrush communities grade into mountain big sagebrush communities.

Table 1—Consistency, frequency, and composition by weight of vascular plant taxa in yellowbrush communities

Plot freq. % (n = 12) Composition by weight (%) (n = 11)

Taxa Site consistency (%) (n = 12) Range Average Range Average

Yellowbrush 100 13–100 73 12–54 26

Slender wheatgrass 100 20–100 79 7–41 17

Letterman needlegrass 100 30–100 79 2–20 11

Yarrow 92 0–94 49 0–7 3

Peavine 92 0–100 41 0–15 7

Mountain brome 58 0–100 25 0–30 5

Sandberg bluegrass 50 0–100 26 0–37 5

Sedges 58 0–77 22 0–6 3

Everywhere aster 50 0–37 7 0–6 1

Potentilla 50 0–52 19 0–11 2

Dandelion 58 0–100 29 0–4 1

Douglas knotweed 50 0–40 15 0–1 <1

Oniongrass 42 0–80 18 0–3 1

Rockcress 42 0–20 4 0–1 <1

American vetch 42 0–40 12 0–1 <1

Muttongrass 33 1–10 2 0–1 <1

Penstemon 33 0–60 12 0–14 2
346 USDA Forest Service Proceedings RMRS-P-21. 2001

Goodrich, Thompson, and Huber A Yellowbrush/Grass Community Type From the Uinta Mountains and Utah Plateaus

Recently burned big sagebrush sites at high elevation can

take on the appearance of yellowbrush/slender wheatgrass

communities. At one site on the Manti-LaSal National

Forest (Baldy Swamp Burn), yellowbrush and Letterman

needlegrass were common after burning. However,

bluebunch wheatgrass (Elymus spicatus) and not slender

wheatgrass was the dominant grass.

Topographic position and elevation are also indicators of

yellowbrush/slender wheatgrass communities. These communities are most common on leeward slopes and/or at elevations

above that commonly occupied by mountain big sagebrush.

These communities appear to occupy sites not as productive

as tall forb communities and often more exposed to wind.

Although they are often on concave slopes, they are more

commonly on convex slopes than are tall forb communities.

Resource Values ________________

Although yellowbrush is often held in low esteem as a

forage plant by association with other members of the

rabbitbrush genus, it is highly selected during parts of the

year by mule deer (Odocoileus hemionus), elk (Cervus elaphus),

cattle (Bos tarus), and sheep (Ovis aries). Dayton (1931)

noted a good representation of this plant by no means

necessarily indicates a deteriorating range. He indicated

carrying capacity of grass communities was likely increased

by presence of this plant.

Stubble height of individual shrubs of yellowbrush monitored over a 10-year period on the face of Mosby Mountain of

the Uinta Mountains has been reduced on an average of

about 50 percent each winter by elk and deer from an

average of 41 cm in the fall to 19 cm in spring (unpublished

data on file at the Supervisors Office, Ashley National

Forest, Vernal, Utah). Observations on the Ashley National

Forest indicate cattle and sheep on the Tavaputs Plateau

commonly use the flowers and upper parts of stems in late

summer and fall after grasses have cured. These observations are consistent with those recorded by the U.S. Department of Agriculture, Forest Service (1937) that the plant is

used by cattle and sheep mostly after the middle of August.

The graminoids of yellowbrush/grass communities have

moderate to high value for elk and livestock forage. There is

often a moderate diversity of forbs associated with these

communities. These forbs are of various resource value.

Yellowbrush/grass communities are often within close

proximity to aspen and/or coniferous tree cover. Thus, they

provide high value elk foraging areas close to hiding cover.

These communities have high potential for uniform dispersion of ground cover, and high percent ground cover.

They often have high value for watershed protection. Where

pocket gophers have cast up much bare soil, infiltration

rates appear to be high and these sites appear to remain

highly capable of maintaining watershed values.

Management Implications ________

Although this is a comparatively minor community type,

it is important to recognize this community type and not

confuse it as a degraded phase of tall-forb communities.

These communities should not be expected to have capabilities of tall forb communities. Although in some cases,

yellowbrush/grass communities develop as seral communities in burned mountain big sagebrush sites, there are areas

where this community is exclusive of sagebrush sites. To

understand capabilities of the land, it is important to recognize yellowbrush community types that have low or no

potential to support sagebrush.

Ground cover appears to be highly influenced by pocket

gophers. Although ground cover was found at over 90 percent at three sites, it was as low as 35 percent at three sites.

Livestock and wild ungulates have used all of the study sites,

and ungulate use is a likely factor in reduced ground cover.

However, the sites with high percent ground cover have a

similar history of grazing to those with low percent ground

cover. A conspicuous difference between sites with low

percent ground cover and those of high percent ground cover

was the abundance of gopher casts. The influence of pocket

gophers on ground cover should not be overlooked when

making evaluations of ungulate grazing.

Yellowbrush communities are indicated to have high

value for watershed stability. This stability has been maintained under light and moderate livestock grazing. These

communities are indicated to have moderate to high capability to support livestock and wild ungulates without loss

of watershed values under light and moderate grazing

intensities.

Yellowbrush is a plant of high resource value especially

where associated with high frequency of grasses and forbs.

It has been recognized with high capacity to withstand

grazing. It is reasonable to expect high abundance, cover,

and production of this plant is to some degree a function of

livestock grazing at the sites where data was taken for this

study. However, this highly competitive plant can be expected at moderate levels in yellowbrush/grass communities

not grazed by livestock. Vigor of graminoids at some sites on

the Ashley National Forest indicates a history of light to

moderate livestock grazing in the past decade or more.

Yellowbrush was as abundant here as it was at other sites

with a history of higher levels of livestock use.

The studies from which the above information was taken

are part of long-term study inventories. The sites can be

revisited. Repeat information has already been collected

from some of these sites. A clear advantage of this approach

is the opportunity to revisit sites in the future to reevaluate

management implications. Interpretations or management

implications made here are based on data collected to date.

Future information might have other implications.

References _____________________

Anderson, L. C. 1986. An overview of the genus Chrysothamnus

(Asteraceae). In: McArthur, E. D.; Welsh, B. L. comps. Proceedings—symposium on the biology of Artemisia and Chrysothamnus;

1984 July 9–13; Provo, UT. General Technical Report INT-200.

Ogden, UT: U.S. Department of Agriculture, Forest Service,

Intermountain Research Station. 29–45.

Dayton, W. A. 1931. Important western browse plants. U.S. Department of Agriculture Miscellaneous Publication 101. Washington,

DC: U.S. Department of Agriculture, Forest Service. 214 p.

U.S. Department of Agriculture, Forest Service. 1937. Range plant

handbook. Washington, DC: U.S. Department of Agriculture,

Forest Service. Variously paginated.

U.S. Department of Agriculture, Forest Service. 1993. Range ecosystem analysis and management handbook. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Intermountain Region. Variously paginated.
USDA Forest Service Proceedings RMRS-P-21. 2001 347

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Darrell N. Ueckert is Regents Fellow and Professor of Rangeland Ecology

and Management, Robert A. Phillips is former Graduate Research Assistant,

and Joseph L. Petersen is Senior Research Associate, Texas Agricultural

Experiment Station, San Angelo, TX 76901-9714; X. Ben Wu is Associate

Professor, Rangeland Ecology and Management Department, Texas A&M

University, College Station, TX 77843-2126.

Rate of Increase of Redberry Juniper

(Juniperus pinchotii) Canopy Cover in

Western Texas: Ecological and Economic

Implications

Darrell N. Ueckert

Robert A. Phillips

Joseph L. Petersen

X. Ben Wu

Abstract—Redberry juniper (Juniperus pinchotii) is a major problem on Texas rangelands, yet little is known about the rate it is

increasing. This study estimated long-term rates of change of

redberry juniper canopy cover on undisturbed sites and adjacent

sites that were either chained or grubbed at five locations in western

Texas. Juniper cover was estimated from positive transparencies of

aerial photographs by the line intercept method using a 10-X

monocular lense with a vernier. Juniper cover increased at an

average rate of 0.37 percentage unit year–1 (range 0.12 to 0.59) on

undisturbed sites from the mid 1950s or early 1960s to the late

1990s (34 to 41 years). Following chaining or grubbing treatments

during 1970 to 1978, juniper cover increased at an average rate of

1.00 percentage unit year–1, which was significantly faster than the

average rate of 0.5 percentage unit year–1 on untreated rangeland

for the same time interval. Juniper cover returned to pre-treatment

levels in an average of 20.6 years (range 11 to 29) following

mechanical control. The annual increment in herbaceous production was predicted at –2 to –4 kg ha–1 (–1.8 to –3.6 lb acre–1) for sites

or periods where juniper cover was increasing at low rates and at

–15 to –23 kg ha–1 (–13 to –21 lb acre–1) where juniper cover was

increasing at high rates. Data from this study suggest that initial or

maintenance control practices should be installed before juniper

cover exceeds about 12 percent.

Redberry juniper (Juniperus pinchotii) infested about 4.7

million ha (12 million acres) of rangeland in Texas in 1982

(Soil Conservation Service 1985), and it is rapidly increasing

in abundance and expanding its geographical range (Ansley

and others 1995). Only about 34 percent of annual rainfall

reaches mineral soil beneath mature redberry junipers

because of interception by the tree canopies and litter layers

(Thurow and Hester 1997). Mature junipers severely impact

the herbaceous vegetation beneath, and on some soils for

considerable distances beyond, their canopies (Dye and

others 1995), thus, forage production declines as juniper

canopy cover increases (Johnson and others 1999; McPherson

and Wright 1990). Knowledge on the rate of increase of

redberry juniper cover is critical to better understanding its

ecology, assessing the economic feasibility of control programs, and scheduling initial and maintenance control practices. The main objective of this study was to determine the

rates of increase of redberry juniper cover on undisturbed

and mechanically treated rangeland in western Texas. Our

hypothesis was that juniper cover increases faster following

mechanical control than on undisturbed rangeland. A secondary objective was to apply the knowledge on the rate of

juniper cover increase to estimate the temporal effects of

redberry juniper cover changes on herbaceous production.

Materials and Methods ___________

Redberry juniper woodlands were studied at five locations

across the northern and western Edwards Plateau of Texas

(fig.1) along an average annual rainfall gradient from 46 to

62 cm (18.1 to 24.5 inches). Two 16.2-ha (40-acre), juniperinfested sites, one with and one without a history of prior

mechanical control that were in close proximity and on the

same soil, were selected at each location. Other criteria for

site selection were that (1) redberry juniper was the dominant overstory species, (2) there were no other large, evergreen plants that could be mistaken for junipers on aerial

photographs taken during winter, (3) maintenance juniper

control treatments had not been applied to treated plots

subsequent to the initial mechanical control treatments,

(4) past management was typical for the region, and

(5) topographical or man-made features facilitated precise

location of the sites on large-scale aerial photographs.

The soils at all study sites were shallow, with rapid surface

runoff, and low to very low water availability. Juniper control

treatments included two-way chaining at three sites (1970

in Coke County, 1972 in Irion County, 1978 in Reagan

County), one-way chaining in 1971 in Crockett County, and

grubbing in 1976 in Nolan County.

Positive transparencies of all available aerial photographs

(scale 1 cm = 79 m) (1 inch = 660 ft) of each site were

purchased from the USDA Farm Services Agency Aerial

Photography Field Office in Salt Lake City, Utah. The

earliest photographs were taken in 1955 and the latest in
348 USDA Forest Service Proceedings RMRS-P-21. 2001

Ueckert, Phillips, Petersen, and Wu Rate of Increase of Redberry Juniper (Juniperus pinchotii) Canopy Cover in Western Texas...

1997. All photographs were taken in winter and redberry

juniper plants or clusters were evident on the photographs

as dark or black areas within the grey matrix of dormant

grasses and bare ground. A 10-X hand lense with a vernier

was used to estimate juniper cover by the line intercept

method (Bonham 1989) on each aerial photograph of each

study site, while the positive transparency was on a light

table. The center one-hundred 0.1-mm (0.0039-inch) increments of the vernier were used for line transects. Forty-five

line transects, equivalent to 79 m (259 ft) in length, were

sampled on each aerial photograph of each site. The mean

canopy cover for each photograph of each site was calculated.

Redberry juniper cover on each study plot was estimated in

the field by the line intercept method in July 1999 for

comparison with estimates from the most recent (1996 or

1997) aerial photographs. Ten 152.4-m (500-ft) line transects

were sampled on each 16.2-ha (40-acre) plot. The mean

canopy cover was calculated for each plot.

The rate of change of juniper cover (percentage units

year–1) for each site was calculated by dividing the percentage point change in cover from photograph A to photograph

B by the number of years that had lapsed between the two

photographs. Live juniper cover remaining subsequent to

chaining or grubbing was assumed to be about 1 percent,

based on our observations of commercial chaining and grubbing operations in the region.

Analysis of variance was used to determine if the estimates of juniper cover for each site from the most recent

aerial photographs and from field sampling in 1999 were

significantly different. Variation among subsamples within

each plot (n = 45 for aerial photographs; n = 10 for field

sampling) was utilized as the estimate of error. Data on

juniper cover from each study site were subjected to analysis

of variance to determine if juniper cover changed significantly during the time interval between photographs.

Variation among subsamples within treatments was utilized as the estimate of error. Means were separated by LSD

at P ≤0.05. Analysis of variance was also used to test for

differences in rates of change of redberry juniper canopy

cover post treatment on chained or grubbed sites and for this

same time interval on untreated plots. Locations (n = 5) were

utilized as replications in this analysis.

We used our estimates of the rates of change of juniper

cover to estimate juniper cover for each year between the

earliest and latest photographs for each undisturbed site.

These yearly juniper cover values were then used in the

natural log model of the relationship between annual herbage production and redberry juniper cover developed in the

Edwards Plateau by Johnson and others (1999) to estimate

the decline in total herbaceous production as a function of

time. This production function is defined as:

 

Y e X = 7 1626024 0 000441 − 2 . .

where Y = annual herbage production in kg ha–1, e is a

transcendental number 2.718282, X = redberry juniper

canopy cover (percent), and r2 = 0.9054.

Results and Discussion __________

Cover Estimates From Photographs

Versus Field Sampling

Estimates of juniper cover from 1996 or 1997 aerial photographs and from field sampling in 1999 were similar for

seven of the 10 study sites, but field estimates were significantly (P ≤0.05) lower than those from photographs for three

sites (data not shown). Visual estimates of juniper cover on

the photographs of these three sites by two observers were

in close agreement with the means obtained from the photographs using the 10-X monocular lense method. We concluded that ten 152.4-m (500-ft) line transects were not an

adequate sample size for field sampling on these three sites

because the juniper was spatially arranged either in patchy

or striated patterns. We feel confident that the 10-X monocular lense method provided acceptable estimates of redberry

juniper cover on all 10 of our study sites.

Juniper Canopy Cover Changes

Undisturbed Rangeland—Juniper cover decreased or

remained relatively static for several years after the mid

1950s on untreated sites where the initial cover was >30

percent (see graphs for Irion and Coke County sites in fig. 2).

In contrast, juniper cover steadily increased, usually at

increasing rates, on undisturbed rangeland where the initial canopy cover was ≤14 percent (see graphs for Crockett,

Nolan, and Reagan County sites in fig. 2). These differences

suggest that, following the drought of the 1950s, intraspecific competition may have suppressed juniper growth and

seedling recruitment on rangeland with heavy juniper cover,

whereas adequate resources were available for juniper growth

and seedling recruitment on rangeland with light juniper

cover.

The rate of juniper cover increase on undisturbed rangeland escalated over time from the mid 1960s through the late

1990s at most sites (fig. 2). Terminal rates of canopy cover

Figure1—Locations of redberry juniper study sites in

the Edwards Plateau, Texas.
USDA Forest Service Proceedings RMRS-P-21. 2001 349

Rate of Increase of Redberry Juniper (Juniperus pinchotii) Canopy Cover in Western Texas... Ueckert, Phillips, Petersen, and Wu

change on undisturbed rangeland varied from 0.45 percentage unit year–1 in Irion County, where cover was approaching 38 percent, to 1.08 percentage unit year–1 in Crockett

County, where cover was approaching only 26 percent (fig. 2).

The Crockett County undisturbed site supported only 11

percent juniper cover in 1985, which was much less than was

present on the other undisturbed sites. This suggests that

the environment of the Crockett County site during 1985 to

1996 was capable of supporting more juniper cover, whereas

juniper populations on the other undisturbed sites were

more mature, and perhaps approaching equilibrium with

their environments.

The long-term rates of change of juniper cover over 34- to

41-year periods on the five undisturbed sites averaged 0.37

percentage unit year–1 (range 0.12 to 0.59). The undisturbed

site in Irion County, which supported the greatest initial

juniper cover (33 percent) (fig. 2), had the lowest long-term

rate of change (0.12 percentage unit year–1). The undisturbed site with the lowest initial juniper cover (6 percent)

exhibited the greatest long-term rate of change in juniper

cover (0.59 percentage unit year–1) (see Crockett County site

in fig. 2). Soulé and Knapp (1999) reported that western

juniper (J. occidentalis spp. occidentalis) cover increased at

rates of 0.08 percentage unit year–1 on an ungrazed site and

at 0.11 to 0.18 percentage unit year–1 on grazed sites during

1951 to 1994 in central Oregon where average annual

precipitation was 25 cm (9.8 inches). The faster development

of redberry juniper woodlands in western Texas may be a

function of greater annual rainfall or to inherent differences

among these two species in growth rate, seed production,

recruitment rates, or the age at which these species reach

reproductive maturity.

Mechanically Treated Rangeland—Redberry juniper

canopy cover increased at an average rate of 1.00 percentage

unit year–1 over the 18- to 26-year periods following chaining

or grubbing (range 0.72 in Reagan County to 1.21 in Irion

County). During this same time interval, the canopy cover of

undisturbed juniper increased at 0.50 percentage unit year–1,

which was significantly (P ≤0.001) lower than the average

rate following mechanical treatments. Short-term rates of

cover change (between photographs) subsequent to mechanical treatments ranged from 0.5 to 1.73 percentage unit

year–1 (fig. 2). Juniper cover increased at similar rates on

sites two-way chained, one-way chained, and grubbed.

The more rapid development of juniper cover following

mechanical treatments can be attributed to three factors.

Redberry juniper seedlings and saplings are often very

abundant in the understory of mature junipers in the Edwards

Plateau (Dye and others 1995; Ueckert and Whisenant

1982), and these small plants are not effectively controlled

by chaining or grubbing. Removal of mature junipers by

chaining or grubbing reduces the interference of mature

junipers with the growth of these juvenile plants, and they

grow very rapidly. On some sites, chaining only removes the

aboveground growth of many redberry junipers, and these

plants resprout from the basal caudex, then grow very

rapidly because of their extensive root system (McPherson

and Wright 1989). Also, the soil disturbance and juniper

debris created by chaining or grubbing provides seedbeds for

juniper seed germination and safe sites for juniper seedling

establishment.

Interrelationship of Juniper Cover,

Herbage Production, and Time

Linear and polynomial models with r2 values >0.998 explained the decline in annual herbage production over time

in response to increasing redberry juniper cover on our five

untreated range sites (fig. 3). Annual herbage production

was predicted to decrease at increasing rates over time at the

Crockett, Nolan, Reagan, and Irion County study sites, and

to decrease at a slightly decreasing rate over time at the

Coke County site. The annual increment in herbage production was low (–2 to –4 kg ha–1 year–1) (–1.8 to –3.6 lb acre–1

year–1) for sites and periods when juniper cover was increasing at low rates (0.15 to 0.32 percentage unit year–1), intermediate (–11 to –14 kg ha–1 year–1 ) (–10 to –12 lb acre–1

year –1) when juniper cover was increasing at intermediate

rates (0.45 to 0.61 percentage unit year–1), and high (–15 to

–23 kg ha–1 year–1) (–13 to –21 lb acre–1 year –1) when juniper

cover was increasing at the highest rate (1.08 percentage

unit year–1). The natural log production function predicted

Figure 2—Redberry juniper canopy cover (percent)

during 1955 to 1997 on undisturbed rangeland and

adjacent sites subjected to chaining or grubbing in

Coke, Crockett, Irion, Nolan, and Reagan Counties,

Texas, estimated from aerial photographs. Numbers

between data points are the rates of canopy cover

change (percentage unit year-1). Means within a line

accompanied by different lower case letters are significantly different at P ≤0.05.
350 USDA Forest Service Proceedings RMRS-P-21. 2001

Ueckert, Phillips, Petersen, and Wu Rate of Increase of Redberry Juniper (Juniperus pinchotii) Canopy Cover in Western Texas...

area, and productivity of the herbaceous undestory, (2) an

influx of subsidiary woody and succulent species, (3) further

reduction in fire frequency and intensity, and (4) a high

incidence and rate of juniper seedling establishment, begin

predominating (Dye and others 1995). Data presented in

this paper document the rates at which redberry juniper

woodlands can develop and recover following chaining or

grubbing, and predicted rates at which herbage production

concomitantly declines. This study substantiates the conclusion of Dye and others (1995) that conversion of juniper

woodlands back to grasslands will not only require initial

reclamation treatments, but also sustained use of followup

maintenance control practices and proper grazing management. Our data show that annual herbage production on

undisturbed rangeland declines slowly as redberry juniper

cover initially reaches 12 to 18 percent, rapidly as juniper

cover increases from 19 up to 29 percent, and slowly on some

sites, but fairly rapidly on other sites, after juniper cover

exceeds 29 percent. We suggest that initial or maintenance

redberry juniper control practices should be installed before

redberry juniper cover exceeds about 12 percent, in other

words, before annual herbage production begins declining at

peak rates.

Knowledge of the rate woody plant canopy cover changes

is essential for determining the economic feasibility of control projects. In a recent study of the economic feasibility of

redberry juniper control using two-way chaining as the

initial treatment and periodic prescribed burning as maintenance treatments, Johnson and others (1999) utilized

empirical linear rates of juniper cover change of 1.6, 2.5, and

5 percentage units year-1 across a range of untreated juniper

cover of 10 to 30 percent and subsequent to two-way chaining

and prescribed burning. Their study showed that net present

values of juniper control treatments increased from $67 to

$130 ha–1 ($27 to $53 acre–1) and that the optimal burning

cycle decreased from 9 to 5 years as the rate of juniper cover

change increased from 1.6 to 5 percentage units year–1. The

slower rates of juniper canopy cover increase that we report

here for untreated and mechanically treated rangeland

suggest that the net present value of controlling juniper

with chaining and periodic burning would be positive, but

substantially less than $67 ha–1 ($27 acre–1), and that the

optimum burning interval would be substantially longer

than 9 years. More recently and based on data from our

study, SoRelle (2000) used rates of redberry canopy cover

increase of 0.12, 0.37, and 1.08 percentage unit year–1 for

undisturbed stands and rates of 0.5, 1.0, and 1.73 percentage unit year–1 subsequent to initial or maintenance control

practices in his study of the economic feasibility of redberry

juniper control. The net present value to a cattle producer for

controlling redberry juniper using two-way chaining as the

initial treatment and hexazinone (3-cyclohexyl-6-(dimethylamino)-1-methyl-1,3,5-triazine-2,4(1H,3H)-dione) individual plant treatments for maintenance control increased

from about $34 to $56 ha–1 ($14 to $23 acre–1) as the rate of

juniper cover increase without treatment increased from

0.12 to 1.08 percentage unit year–1. The net present value of

juniper control decreased from about $54 to $25 ha–1 ($22 to

$10 acre–1) when the rate of canopy cover increase following

treatment increased from 0.5 to 1.73 percentage unit

year–1.

Figure 3—Relationships between annual herbage

production (kg ha–1) (Y) and time (years) (X) for

undisturbed redberry juniper study sites in Crockett

(1963 to 1997), Nolan (1957 to 1996), Reagan (1961

to 1996), Irion (1964 to 1996), and Coke (1973 to

1996) Counties, Texas. The trend lines were developed by integrating our estimates of annual redberry

juniper canopy cover (percent) into a natural log

model of the relationship between annual herbage

production and redberry juniper canopy cover developed in the northern Edwards Plateau, Texas, by

Johnson and others (1999). Functional forms were

fitted to the trend lines that had r2 values >0.998.

Annual juniper canopy cover (dotted line) is included

in each graph for reference only.

that herbage production on our five untreated sites had

decreased by an average of 272 kg ha–1 (243 lb acre–1) (range

204 to 320 kg ha–1) or 26 percent (range 17 to 38 percent)

from the mid 1950s or 1960s to the late 1990s.

Management Implications

The threshold from grasslands, in which graminoid-driven

successional processes predominate, to redberry juniperdominated woodlands is crossed when sufficient numbers of

junipers become established and reach reproductive maturity. At this point, juniper-driven successional processes,

including (1) a major reduction in diversity, density, basal
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Rate of Increase of Redberry Juniper (Juniperus pinchotii) Canopy Cover in Western Texas... Ueckert, Phillips, Petersen, and Wu

References _____________________

Ansley, R. J.; Pinchak,W. E.; Ueckert, D. N. 1995. Changes in

redberry juniper distribution in northwest Texas (1948–1992).

Rangelands 17:49–53.

Bonham, C. D. 1989. Measurements for terrestrial vegetation. John

Wiley & Sons, Inc. New York, NY.

Dye, K. L., II; Ueckert, D. N.; Whisenant, S. G. 1995. Redberry

juniper: herbaceous understory interactions. J. Range Manage.

48:100–107.

Johnson, P.; Gerbolini, A.; Ethridge, D.; Britton, C.; Ueckert, D.

1999. Economics of redberry juniper control with burning in the

Texas Rolling Plains. J. Range Manage. 52:569–574.

McPherson, G. R.; Wright, H. A. 1989. Direct effects of competition

on individual juniper plants: a field study. J. Appl. Ecol. 26:

979–988.

McPherson, G. R.; Wright, H. A. 1990. Effects of cattle grazing and

Juniperus pinchotii canopy cover on herb cover and production in

western Texas. Amer. Midl. Natur. 123:144–151.

Soil Conservation Service. 1985. Texas brush inventory. USDASCS. Temple, TX.

SoRelle, J. 2000. Economic feasibility of redberry juniper control

using individual tree treatments. M.S. Thesis. Texas Tech Univ.

Lubbock, TX.

Soulé, P. T.; Knapp, P. A. 1999. Western juniper expansion on

adjacent disturbed and near-relict sites. J. Range Manage. 52:

525–533.

Thurow, T. L.; Hester, J. W. 1997. How an increase or reduction in

juniper cover alters rangeland hydrology, In: C.A. Taylor, Jr.

(ed.). Proc. 1997 Juniper Symposium. Texas Agr. Exp. Sta. Tech.

Rep. 97-1. San Angelo, TX: 4:9–22.

Ueckert, D. N.; Whisenant, S. G. 1982. Individual plant treatments

for controlling redberry juniper seedlings. J. Range Manage.

35:419–423.
352 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Stephan A. Nelle is Wildlife Biologist, Natural Resources Conservation

Service, 3812 Sherwood Way, San Angelo, TX 76901.

Ecological Implications of Using Goats

for Control of Juniper in Texas

Stephan A. Nelle

Abstract—The Edwards Plateau region of central Texas supports

a rich diversity of plants and animals. The diversity and abundance

of trees and shrubs is especially noteworthy, but two species of

juniper (Juniperus ashei, Juniperus pinchotii) now dominate much

of the landscape. Goats are currently being recommended to control

juniper infestations. The concept of using biological methods for the

control of nuisance plant species has gained much attention in

recent years. Some claim that biological control is more environmentally friendly and cost effective than herbicides or heavy equipment. Because juniper is one of the poorest browse plants in the

region, other more desirable shrubs are browsed in preference to

juniper. While goats can be managed to cause damage or even death

to juniper, this level of browsing is very detrimental to a host of more

palatable shrubs and trees. These more palatable species become

stunted and unproductive and often die prematurely when subjected to this kind of browsing. Reproduction is impaired and

eventually they are lost from the local plant community. These

harmful side effects of biological juniper control are not often

considered by practitioners. These side effects are easily observed,

but have not been scientifically studied nor quantified.

Background and History _________

The Edwards Plateau region of Texas is a 24 million acre

area that lies in the central and southwestern portion of the

State. The region is characterized by rolling to steep topography, shallow, rocky, limestone soils, and receives 14 to 32

inches of rainfall on a west to east gradient. The region is

biologically very diverse being the transition between forests to the east and deserts to the west and between grasslands to the north and thorn shrublands to the south. There

are about 2,500 species of vascular plants native to the

region (Hatch and others 1990).

The historic climax plant communities varied greatly,

depending on soils, topography, rainfall, and the extent of

natural fire. Historic landscapes included mid grass prairies

on the flatter divides, oak savannas across the rolling uplands, juniper-oak woodlands in the canyonlands and steep

terrain, and riparian forests. Most natural resource professionals agree that periodic and recurring wildfire was responsible for maintaining the open character of the prairie

divides and the rolling oak savannas (Smeins 1980). This

fact was recognized in the early 1900s (Bray 1904; Foster

1917).

The presence and extent of juniper in pre-settlement

times has been hotly debated and argued by ranchers,

natural resource managers, ecologists, and environmentalists. Despite the ongoing debate, the historical record is

abundant and clear that juniper was common and dominated some sites, and was uncommon or absent on other

sites (Curtis 2000; Smeins 1980; Weniger 1984)

The region is almost entirely privately owned ranches and

has been grazed by domestic livestock for over 100 years.

Various combinations of cattle, sheep, goats, exotic ungulates, and native white-tailed deer are present across the

region and are the basis of the ranching and hunting economy.

Because of poor grazing management and the resulting

reduction in fires, the vegetation and general appearance of

the region has changed dramatically over the past century

(Smeins and others 1997). Herbaceous cover has been degraded by heavy and continuous grazing. Tall and mid

grasses and desirable forbs have been eliminated or greatly

reduced in most pastures. A sparse ground cover of low

successional species and excessive bare ground has caused

poor infiltration, accelerated runoff, and erosion. The lack of

adequate fine fuel has greatly reduced the opportunity for

natural or prescribed fire.

Juniper Encroachment

As grasslands were thinned by heavy and continuous

grazing, fires were not able to burn with the intensity or at

the scale and frequency required to suppress and control

increases in woody plants. Several species of woody plants

including two species of juniper have taken advantage of this

opportunity. Red-berry juniper (Juniperus pinchotii) and

Ashe juniper (Juniperus ashei) have increased in extent in

response to the overgrazing and subsequent lack of fire.

Rangeland managers often refer to this as an “invasion” as

if juniper had some insidious power to overwhelm healthy

grasslands. Others consider the increase of juniper merely a

natural ecological response to a man-made disturbance.

The spread and increase of juniper into what formerly

were grasslands and savannas has caused problems for the

rancher. The cover of grass that had already been altered by

grazing practices was being weakened further by increases

in juniper. The shading of grasses by the juniper canopy, the

competition for moisture, and the interception of rainfall all

contribute to the progressive loss of grass cover and forage

(Thurrow and Carlson 1994; Ueckert 1997). The inability of

the rancher to see and manage livestock is also impaired by

increases in juniper. Several million acres of once productive

grazing land now supports dense canopies of juniper and

sparse densities of grass.
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The Ecological Implications of Using Goats for Control of Juniper in Texas Nelle

Juniper Control

Since increases in juniper were first observed, ranchers as

well as agricultural and conservation agencies have been

busy discovering and promoting methods to control juniper

(Wolff 1948). Many different methods have been used and

millions of dollars spent to kill juniper. Mechanical methods

including grubbing, dozing, chaining, and rootplowing with

large equipment have been popular (Scifres 1980). Hand

cutting of ashe juniper, a nonsprouting species has long been

used and is effective. Chemical methods have been tried but

with limited and small scale success. The use of prescribed

fire is gaining in popularity, yet most landowners are either

unwilling or unable to use this method, and less than onetenth of 1 percent of the acreage in the region is burned each

year (Nelle, unpublished data).

Regardless of the method of control or the effectiveness of

control, one thing is certain: juniper begins to reappear and

increase soon after it has been removed. Many areas within

the Edwards Plateau have had all juniper removed several

different times in the past 50 years only to see it return to

undesirable densities. In the ecological tussle for control of

the landscape, juniper is winning and healthy grasslands

are loosing.

Goats _________________________

Goats have been numerous in the region for over 100

years. The Edwards Plateau has led the country in goat

production ever since records have been kept. Goat numbers

reached their peak in the mid 1960s with about 4 million

head. Since that time, goat numbers have declined (Findley

1990). Goat numbers on individual ranches are commonly

as high as one goat per 3 to 5 acres.

Diet and food habit studies have confirmed that goats eat

large amounts of browse even when other kinds of forage are

available (Bryant and others 1979). The rich diversity and

the abundance of desirable woody plants in the Edwards

Plateau have provided a natural resource base for a thriving

goat industry. When managed on a renewable basis the

raising of goats can be very compatible with the sustainability of the browse resource (NRCS 1994)

Are Goats Nature’s Herbicide?

Some agricultural professionals have been making the

claim in the popular media that goats are “nature’s herbicide” and an “environmentally friendly” way to control

juniper. The word, “herbicide” literally means “plant killer.”

It is true that goats or any other kind of livestock can be

managed intentionally or unintentionally in a way that

causes harm to plants. Grazing or browsing an excessive

amount of leaf material will necessarily reduce the photosynthetic ability of a plant to sustain itself. If this excessive

level of leaf removal continues, plants will be reduced in

vigor and can eventually be killed. When this process is

unintentional and unplanned, it is called overgrazing or

overbrowsing. When it is planned, it is often called biological

control.

There is an important distinction between the normal

consumption of juniper by goats and the biological control of

juniper. Goats and deer will naturally consume some juniper

as a part of their diet, especially in winter when the availability of other green browse is limited. This degree of

normal browsing is not heavy enough to exert physiological

damage to established plants although some seedling mortality is likely to occur.

Side Effects

When any land management practice is considered, it is

wise to evaluate the potential negative side effects prior to

full-scale endorsement (Hughs 2000). If a practice successfully meets the intended objective and if associated side

effects are minimal or tolerable, the practice might be safely

prescribed. If the practice meets its objective, but there are

serious unintentional side effects, the practice would at least

be considered questionable. The consequences of the side

effects would be weighed against the benefits before the

practice is recommended. In the case of biological control of

juniper with goats, the ecological side effects are substantial.

Juniper is one of the least preferred browse plants of the

region. The secondary chemical compounds in the leaves

make juniper relatively unpalatable to browsing animals

(Launchbaugh and others 1997). This built-in defense mechanism against browsing is one reason why juniper has proliferated in the face of large numbers of browsing goats and

deer. Even though juniper is nonpreferred and relatively

unpalatable, goats can be managed for an unnaturally high

consumption of juniper, even to the point of causing injury

and death of juniper.

Goats, like most other herbivores are selective feeders.

They will selectively consume the best, most palatable

plants in preference to less palatable plants. As the more

preferred plants become heavily browsed, goats will move to

progressively less and less preferred plants. A host of more

palatable woody plants will be very heavily browsed when

goats are forced to eat unnaturally high amounts of juniper

(table 1). When such heavy use continues over a sustained

period, the woody plant diversity of the area suffers loss.

Although most ranchers agree that there are many desirable

kinds of shrubs and trees, their dislike of a few brush species

such as juniper often overshadows their desire to manage

the beneficial species.

An experienced observer can easily discern this loss or

reduction of desirable woody species across the region.

Decades of heavy goat grazing have caused distinct browse

lines on preferred and moderately preferred species. All

growth within reach of animals is consumed. Shorter plants

exhibit severe hedging, a reduction in leaf size, dead twigs

and branches, and an overall reduction in vigor. Flowering

and seed production is curtailed. Successful reproduction, if

it occurs at all, is limited to protected sites where goats and

deer cannot browse. This reduction of plant diversity is one

of the major side effects of this practice.

Ecological Implications

The reduction of plant diversity is a fairly clear side effect

of heavy goat browsing. The long term ecological implications of this loss are less clear but should be considered.

There has been little or no research in this area. In the
354 USDA Forest Service Proceedings RMRS-P-21. 2001

Nelle The Ecological Implications of Using Goats for Control of Juniper in Texas

absence of unbiased scientific studies, general knowledge,

common sense, and experience must be used to consider

what the implications may be. A reduction in native plant

diversity has the probability of impacting native wildlife

diversity. Changes in specific cover requirements and the

diversity of food items may affect a whole array of bird

species. Simplified plant communities are usually less stable

and resilient than more diverse communities. Energy and

mineral cycling through an ecosystem is impaired when

plant diversity suffers. Soil microbes, soil tilth, and soil

stability may be affected when plant communities change.

Riparian health and stability are most certainly impacted

with a loss of key woody species. Consequently, water quality and fish habitat are affected. Indirectly, gradual damage

to the natural resource base (soil, water, plants, animals) will

lead to insufficient economic returns from ranching and landowners may be forced to subdivide and sell off native ranges

for the profits of commercial and residential development.

A Holistic Perspective____________

Natural resource managers would be wise to take a long

term, wide-angle look at land management practices before

they are recommended (White 2000). Instead of looking at a

single facet of a problem (such as an increase in juniper) and

a simple solution, managers need to take a more ecologically

holistic view (Nelle 1997). Considering the causes of a

problem, distinguishing between symptoms and root causes,

and discovering the possible side effects of various treatments are essential elements of wise land management. In

the case of juniper and its control with goats, the following

considerations are important in gaining a holistic perspective:

1. Juniper–oak woodlands are the native climax vegetation type on certain sites in the region. Juniper control

on these sites is ecologically questionable.

2. Juniper has encroached and increased on other sites

where it was not a part of the climax vegetation.

3. Under conditions of overgrazing, the increase of juniper

is the natural ecological response and provides a degree

of protection to the site.

4. Juniper encroachment is due directly to a reduction in

fires and indirectly to overgrazing, which prevents the

buildup of adequate fine fuel.

5. The increase of juniper to undesirable densities causes

significant problems for ranching.

6. The control of juniper where it has encroached should

only be considered after a long term commitment has

been made to proper grazing management.

7. The periodic use of fire to control small encroaching

juniper is strongly encouraged.

8. Goats can be managed to exert some control of juniper,

but at the expense of many other desirable woody

species.

9. Maintaining the native plant diversity of a site is important to wildlife habitat, soil health, watershed function,

ecological stability, and economic viability.

References _____________________

Bray, W. L. 1904. The timber of the Edwards Plateau of Texas. U.S.

Department of Agriculture, Bureau of Forestry, Bulletin No. 49.

30 p.

Bryant, F. C.; Kothman, M. M.; Merrill, L. B. 1979. Diets of sheep,

Angora goats, Spanish goats and white-tailed deer under excellent range conditions. Journal of Range Management. 32:

412–417.

Curtis, David C. 2000. Protecting endangered ecosystems of the

Edwards Plateau. In: Brush, water and wildlife symposium:

proceedings; 2000 Novemer 30–December 1. Kerrville, TX: 101–

111.

Findley, D. S. 1990. 1867–1990 Texas historic livestock statistics.

Texas Agricultural Statistics Service. Austin, TX. 92 p.

Foster, J. H. 1917. The spread of timbered areas in central Texas.

Journal of Forestry. 15:442–445.

Hatch, S. L.; Gandhi, K. N.; Brown, L. E. 1990. Checklist of the

vascular plants of Texas. Texas Agricultural Experiment Station.

MP-1655. 158 p.

Hughs, S. K. 2000. Brush management, water and wildlife: a

checklist for ecosystem management. In: Brush, water and wildlife symposium: proceedings; 2000 November 30–December 1.

Kerrville, TX: 96–97.

Launchbaugh, K. C.; Taylor, C. E.; Straka, E.; Pritz, R. 1997.

Juniper as forage: an unlikely candidate. In: Juniper symposium:

proceedings; 1997 January 9–10. San Angelo, TX: 7.3–7.9.

Table 1—A partial listing of desirable woody plants that are browsed in

preference to juniper and that may be lost under heavy

browsing.

Common name Scientific name

Texas kidneywood Eysenhardtia texana

Littleleaf leadtree Leucaena retusa

Texas sophora Sophora affinis

Carolina buckthorn Rhamnus caroliniana

Mountain mahogany Cercocarpus montanus

Texas mulberry Morus microphylla

White honeysuckle Lonicera albiflora

Black cherry Prunus serotina

Hawthorne Crataegus crusgallii

Rusty blackhaw Viburnum rufidulum

Inland ceanothus Ceanothus herbacea

Texas oak Quercus texana

Netleaf hackberry Celtis reticulata

Cedar elm Ulmus crassifolia

American elm Ulmus americana

Black willow Salix nigra

Bumelia Bumelia languinosa

Clematis Clematis drummondii

Roemer acacia Acacia roemeriana

Wild plum Prunus angustifolia

Redbud Cercis canadensis

Grapevine Vitis sp.

Virginia creeper Parthenocissus quinquefolia

Greenbriar Smilax bona-nox

Carolina snailseed Cocculus carolinus

Western soapberry Sapindus drummondii

Elbowbush Forestiera pubescens

Ephedra Ephedra antisyphyllitica

Live oak Quercus virginiana

White shin oak Quercus durandii

Vasey shin oak Quercus pungens

Blackjack oak Quercus marylandica

Skunkbush sumac Rhus trilobata

Evergreen sumac Rhus virens

Littleleaf sumac Rhus microphylla

Flameleaf sumac Rhus copallina

Feather dalea Dalea formosa

Roughleaf dogwood Cornus drummondii

Buttonbush Cephalanthus occidentalis
USDA Forest Service Proceedings RMRS-P-21. 2001 355

The Ecological Implications of Using Goats for Control of Juniper in Texas Nelle

Nelle, S. 1997. A holistic perspective on juniper. In: Juniper symposium: proceedings; 1997 January 9–10. San Angelo, TX: 4.3–4.8.

Natural Resources Conservation Service. 1994. The use and management of browse in the Edwards Plateau of Texas. Temple, TX.

8 p.

Scifres, C. J. 1980. Brush management, principles and practices for

Texas and the Southwest. Texas A&M University Press, College

Station, TX. 360 p.

Smeins, F. E. 1980. Natural role of fire on the Edwards Plateau. In:

Prescribed burning of the Edwards Plateau of Texas. Texas

Agricultural Extension Service. College Station, TX: 4–16.

Smeins, C. J.; Fuhlendorf, S.; Taylor, C. 1997. Environmental and

land use changes: a long-term perspective. In: Juniper symposium: proceedings; 1997 January 9–10. San Angelo, TX: 1.3–1.21.

Thurow, T. L.; Hester, J. W. 1997. How an increase or reduction in

juniper cover alters rangeland hydrology. In: Juniper symposium: proceedings: 1997 January 9–10. San Angelo, TX: 4.9–4.22.

Ueckert, D. N. 1997. Juniper control and management. In: Juniper

symposium; proceedings: 1997 January 9–10. San Angelo, TX:

5.23–5.34.

Weniger, D. 1984. The explorers’ Texas. Eakin Press, Austin, TX.

224 p.

White, L. D. 2000. Integrated management for water, brush and

wildlife on Texas rangelands. In: Brush, water and wildlife

symposium: proceedings; 2000 November 30–December 1.

Kerrville, TX: 77.1–77.12.

Wolff, S. E. 1948. An evaluation of some weedy Texas junipers. U.S.

Department of Agriculture, Soil Conservation Service. Ft. Worth,

TX: 89 p.
356 USDA Forest Service Proceedings RMRS-P-21. 2001

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Martha Martín-Rivera and Fernando Ibarra-Flores are Range Scientists,

INIFAP-CIRNO, Blvd. del Bosque # 7 Fracc. Valle Verde, Hermosillo, Sonora,

Mexico, CP 83200. Fred S. Guthery is Wildlife Specialist, Department of

Forestry, Oklahoma State University, 008 Agricultural Hall, Room C,

Stillwater, OK 74078-6013. William P. Kublesky, Jr., is Wildlife Specialist,

Buenos Aires National Wildlife Refuge, P.O. Box 109, Sasabe, AZ 85633.

Gustavo Camou-Luders is a Producer, Rancho El Carrizo, Sierra Murrieta

No. 168, Col. Loma Linda, Hermosillo, Sonora, CP 83150. Jesus FimbresPreciado is a Producer, Rancho Grande, Veracruz No. 33 Ote. Hermosillo,

Sonora, CP 83200. Donald Jonson-Gordon is Professor of Range Management, UNISON-Departamento de Agricultura y Ganaderia. Km 21 Carretera

a Bahia Kino, Hermosillo, Sonora, Mexico.

Abstract—Native vegetation of semiarid grasslands and desert

ecosystems that comprise the Arbosufrutescent Desert scrub vegetation in north-central Sonora has been degraded by overgrazing,

drought, farming, woodcutting, and a host of other activities over

the past century. Several studies were conducted at “Rancho Grande”

and at “Rancho El Carrizo,” Sonora from 1992 to 1999 to evaluate

the effect of several range improvement practices on wildlife habitat. Twenty-five-thousand seedlings of eight native shrubs and

trees were transplanted on a site in north-central Sonora. Survival

rates among species varied from 55 to 84 percent 1 year after

transplanting and from 10 to 41 percent 3 years after planting. Reestablishment of native shrubs represents a promising technique

that could restore native woody vegetation on degraded ecosystems

that lack diversity. Habitat management by disking and shredding

coupled with improvement in grazing management with shortduration grazing, have also resulted in improved native herbaceous

conditions on thousands of acres of private ranches. These results

are encouraging. The potential impact that re-establishment of

native shrubs, control of undesirable brush species, and improvements in grazing management may have on wildlife occupying

rangelands in north-central Sonora will be discussed.

Introduction ____________________

Extensive areas of desert rangelands that were once

productive are now highly infested with less desirable brush

species and toxic plants (Vallentine 1971). Overgrazing,

droughts, frosts, accidental fires, land clearing for farming

and grazing; and the extensive use of wood for fuel, fences,

Habitat Improvement for Wildlife

in North-Central Sonora, Mexico

Martha Martín-Rivera

Fernando Ibarra-Flores

Fred S. Guthery

William P. Kublesky, Jr.

Gustavo Camou-Luders

Jesus Fimbres-Preciado

Donald Johnson-Gordon

charcoal, and wood carving have caused drastic changes in

the vegetation, resulting in low forage productivity, unprotected soils, and a high susceptibility for soil erosion (Scifres

1980; Ibarra and others 1996). Reduction of cattle numbers

and good grazing management alone may not be sufficient to

restore productivity on these deteriorated rangelands. In

most cases range seeding with high quality grasses and

shrubs may be the best alternative for restoring productivity

(Vallentine 1971; Ibarra and others 1996). Browse species

are important because they are a good source of food for

humans, livestock, and wildlife; provide shelter, soil protection, and soil stabilization; improve soil fertility; and provide

a favorable microhabitat for the establishment of other

species (Whisenant and others 1982; Guthery 1986; Ibarra

and Martin 1995).

Buffelgrass (Cenchrus ciliarisL.) is a warm season bunchgrass widely used in much of Mexico for revegetation following brush removal. Forage production of buffelgrass exceeds

that of native grasses and stocking rates are frequently

three to ten fold greater than on native rangelands (Martin

and others 1995). Brittlebush (Encelia farinosa A. Gray) is

a deciduous half shrub native to the Sonoran Desert (Benson

and Darrow 1981), which infests buffelgrass stands. Densities of this species have almost doubled in 30 years on

rangelands near Tucson, Arizona (Shreve and Hinckley

1937), and densities as high as 30,000 plants per hectare

have been reported in buffelgrass seeded pastures in Sonora,

Mexico (Ibarra and others 1986). High resin and oil contents

make brittlebush a plant of low palatability for cattle and

wildlife. As the species increase, density, cover, and forage

production of buffelgrass declines (Ibarra and others 1996).

Masked bobwhite (Colinus virginianus ridgwayi) is an

endangered specie restricted to the Buenos Aires National

Refuge in Arizona, U.S.A., and to rancho El Carrizo and

Rancho Grande in Sonora, Mexico. Densities of masked

bobwhite have been drastically declining in the last 20

years, with an actual estimated bird population of close to

3,000 at these three locations. As a result, ranchers and

range managers of both countries are applying grazing

management and range improvement practices to restore

bird population. Additionally, densities of Sonoran mule

deer (Odocoileus hemionus eremicus) have been drastically

declining in some ranches because of severe droughts,

deficient range management practices, and poor wildlife

management strategies.
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Habitat Improvement for Wildlife in North-Central ... Martín-Rivera, Ibarra-Flores, Guthery, Kublesky, Camou-Luders, Fimbres-Preciado, and Johnson-Gordon

There is a lack of information on the establishment of

browse species for cattle and wildlife in the Sonoran Desert.

Also, there is not enough information about the effect of

vegetation manipulation by mechanical control of unpalatable shrubs and grazing on range productivity and animal

responses. A series of range improvement practices were

conducted at “Rancho Grande” and “Rancho El Carrizo”

from 1992 to 1999 with the following objectives: (1) to

evaluate the seeding potential of several browse species by

transplanting to restore range productivity, (2) to evaluate

the effect of vegetation manipulation by mechanical means

to increase forage production for cattle and wildlife, (3) to

evaluate the effect of grazing systems on wildlife habitat

recovery, and (4) to enhance species diversity and productivity for livestock and wildlife.

Material and Methods ____________

The Rancho Grande site (29° 49' N Lat. and 111° 14' W

Long.) is located 90 Km north of Hermosillo, Sonora, Mexico

(fig. 1), at an elevation of 700 m on a gently sloping terrain

(<5 percent). Mean annual precipitation is 320 mm, 75

percent of which occurs during the summer. Mean annual

temperature is 24.5 °C, with a frost-free period of 345 days.

Soils are deep sandy loams of granitic origin, with moderate

permeability and a pH of 7.0.

The Rancho El Carrizo site (30° 0' N Lat. and 111° 12' W

Long.) is located 120 Km north of Hermosillo, Sonora,

Mexico (fig. 1), at an elevation of 750 m on a gently sloping

terrain (<5 percent). Mean annual precipitation is 330 mm,

75 percent of which occurs during the summer. Mean annual

temperature is 24.0 °C, with a frost-free period of 345 days.

Soils are deep sandy loams and deep gravelly loams of

granitic origin, with moderate permeability and a pH of 7.0.

Transplanting Browse Species

A study site was selected within the Arbosufrutescent

Desert shrub vegetation type in the northwestern area of

Sonora, Mexico. The site was located at Rancho Grande on

a recently planted buffelgrass pasture. Twelve-thousand

plants were transplanted in July 1996. Species planted were

selected based on previous animal preference trails. Seed

used for plant propagation was collected 1 year before at

each study site. Plants were grown during 1 full year under

nursery conditions before transplanting to achieve a height

of 20 to 75 cm. Browse species were distributed randomly

and planted every 5 m along contour furrows 40 cm in depth.

Furrows were made at 20 to 50 m intervals with a back

mounted “v” type plow pulled by a bulldozer.

Species were planted by hand on the bottom of the furrows

using shovels. Species planted were: native mesquite

[(Prosopis juliflora) (Swartz) DC.] , chilean mesquite [Prosopis

chilensis (Molina) Stuntz emend. Burkart], ironwood (Olneya

tesota A. Gray), blue palo verde (Cercidium floridum

Bentham), foothill palo verde [Cercidium microphillum

(Torr.) Rose & Johnston], jojoba [Simmondsia chinensis

(Link) Schneid], fourwing saltbush [Atriplex canescens

(Pursh) Nutt.], and zamota (Coursetia glandulosa A. Gray).

The site was fenced to protect it from cattle grazing. Plant

survival (percent) and height (cm) were measured during

the peak growing season of 1996 to 1999 by checking 100

previously marked plants by species.

Shredding for Brittlebush Control

in Buffelgrass Pastures

This study was conducted at Rancho Grande on three

adjoining buffelgrass pastures, 200 hectares each, in poor to

regular condition. Pastures were shredded once during

1995, 1996, and 1997. Shredding at a height of 5 cm was

conducted in April with a 5 m wide flail shredder powered by

a tractor. Initial brittlebush density was 17,570 ± 3,125

plants per hectare, and canopy cover was 46 ± 8.4 percent

across pastures. Initial buffelgrass density was 1.3 ± 0.4

plants per hectare, and basal cover was 5.2 ± 0.6 percent

across pastures. Vegetational changes were monitored on

three 10 x 20 m plots. Total grass and shrub density was

estimated on three 10 m2 permanent quadrats, and cover on

three 20 m long transects per plot (Canfield 1941). Total

forage production was estimated at the end of the summer

growing season in each plot by clipping ten 1 m2 quadrats per

plot. Forage samples were oven dried at 65 °C for 72 hours

and results were expressed in dry matter.

Improving Native Rangelands Infested

With Brush by Disk Harrowing

Two thousand hectares of rangelands, dominated by the

arbosufrutescent brush type, in poor to regular condition Figure 1—Location of study sites, Sonora, Mexico.
358 USDA Forest Service Proceedings RMRS-P-21. 2001

Martín-Rivera, Ibarra-Flores, Guthery, Kublesky, Camou-Luders, Fimbres-Preciado, and Johnson-Gordon Habitat Improvement for Wildlife in North-Central ...

and highly infested with catclaw mimosa [Mimosa laxiflora

(Swarts.) DC.] and creosotebush [Larrea tridentata

(Moc.&Sesse.) Cov.)], were improved by disk harrowing at

rancho “El Carrizo” from 1992 to 1997. Disking at a depth of

20 cm was conducted from March to June by using a disk

harrow with 36 disks mounted on the back of a D-4 bulldozer.

Mainly catclaw mimosa and creosotebush were selectively

controlled by disking, because about 40 percent of the total

vegetation cover was composed of these species. Desirable

brush and tree species protected during disking were blue

palo verde, foot hill palo verde, mesquite, and ironwood. Main

grass species present were three awn (Aristida spp.), 6 weeks

needle grama [Bouteloua aristidoides (H.B.K.) Griseb], and

rothrock grama (Bouteloua rothrockii Vasey). Total dry

forage production was low and averaged 350 kg per hectare.

Treated areas were protected during a full year from cattle

grazing, and they were grazed light to moderate thereafter.

Forage production on disked pastures was estimated at

the end of the summer growing season by clipping. Forage

production increases by disking were compared with forage

production in adjacent untreated pastures. Mortality of

catclaw mimosa and creosotebush was estimated by comparing plant densities inside and outside the treated pastures. Masked bobwhite quail densities were estimated by

direct observation and by call counts. Quail density increases in disked pastures were compared against bird

densities estimated on adjacent untreated pastures. Densities of Sonoran mule deer on treated pastures was estimated by direct animal counting and population changes

over time were compared with deer densities on untreated

adjacent pastures.

Adopting Grazing Systems for Habitat

Improvement

This study was conducted at rancho El Carrizo from 1992

to 1998. The two-thousand hectares of rangelands treated by

disk harrowing to improve masked bobwhite quail habitat

were subdivided into 12 small pastures. Pasture sizes varied

from 140 to 200 hectares. A modified short-duration grazing

system (SDG) was implemented in the ranch to control

grazing. Stocking rates were set following biologists recommendations to remove no more than 60 percent of the total

dry forage production available during the summer growing

season of a given year. Grazing periods are set to be 7 days

in each pasture during the summer growing season, and 15

days of grazing in each pasture during the rest of the year.

Forage production in the SDG was estimated at the end of

the summer growing season by clipping. Forage production

and stocking rate increases on the SDG were compared

against forage production and stocking rates in adjacent

pastures subjected to continuous grazing. Masked bobwhite

quail densities were estimated by direct observation and by

call counts. Quail density increases in the SDG pastures

were compared to bird densities estimated on adjacent

untreated pastures. Densities of Sonoran mule deer on

pastures subjected to SDG were estimated by direct animal

count and population changes over time were compared to

deer densities in adjacent pastures subjected to continuous

grazing.

Results and Discussion __________

Transplanting Browse Species

Total precipitation at “Rancho Grande” was 317, 353, 384,

and 162.5 mm during 1996, 1997, 1998, and 1999 and was

close to the long-term average of (320 mm). In general,

growing conditions during all summers were adequate for

species survival and growth. Precipitation distribution was

adequate during all years, except for the summer of 1996,

the year of planting, when more than 60 percent of the total

rain occurred during the winter. Because of the dry conditions prevailing during the year of planting, approximately

10 liters of water were added to each plant during the

summer of 1996.

Plant survival was different among species after the dry

growing season of 1996, and varied from 55 to 84 percent.

Between the winter of 1996 and the summer of 1999, 51 to

82 percent of the plants were killed by drought and insects

and cattle grazing. Plant survival was different among

species by the end of the summer growing seasons of 1997,

1998, and 1999. Species with the greatest survival rate after

planting in the four summer growing seasons were native

mesquite, chilean mesquite, foothill palo verde, blue palo

verde, and ironwood with 41, 35, 33, 30, and 27 percent

survival, respectively. Species with the lowest survival were

zamota, fourwing saltbush, and jojoba, with 25, 15, and 10

percent survival, respectively.

Plant height was not different among species after the

summer of 1996, but it differed in the summer growing

seasons of 1997, 1998, and 1999. The height of transplanted

species increased from 13 to 138 cm during the four summer

growing seasons after planting. Species that achieved the

greatest height were chilean mesquite and native mesquite

with 138 and 137 cm, respectively. Jojoba had the lowest

height with an average of 13 cm, and the height of the

remaining species varied from 30 to 68 cm.

High densities of Sonoran mule deer, white tailed deer

(O. virginianus couesi), javelina (Tayassu tajacu), and jackrabbit (Lepus alleni) were common at the study site. Low

forage availability outside the exclusions during the dry

period caused severe wildlife grazing on most planted species. Chilean mesquite (with no thorns), jojoba, and fourwing

saltbush were the most preferred species by wildlife. Ten to

25 percent of the fourwing saltbush and jojoba plants were

uprooted by wildlife within 3 weeks of planting.

Survival of transplanted shrubby forage species was adequate in the Sonoran Desert when planting was followed by

a summer with below average precipitation. Mortality of the

browse species was principally due to low moisture availability during the study period, grasshopper consumption,

and wildlife grazing. Similar results have been reported

with other browse species on rangelands (Whisenant and

others 1982; Ueckert and others 1982), although greater

plant survival can be expected in years with above average

precipitation (Springfield 1970).

Results obtained show that browse consumption by wildlife may be an important factor affecting species survival

after transplanting. Similar results had been reported with

different browse species (Springfield 1970; Whisenant and

others 1982). Watering transplanted species during drought
USDA Forest Service Proceedings RMRS-P-21. 2001 359

Habitat Improvement for Wildlife in North-Central ... Martín-Rivera, Ibarra-Flores, Guthery, Kublesky, Camou-Luders, Fimbres-Preciado, and Johnson-Gordon

may be risky because plants with green foliage will attract

more wildlife. Based on survival and growth characteristics,

native mesquite, chilean mesquite, ironwood, blue palo

verde, and foothill palo verde appear to have the greatest

potential for range seeding in the Sonoran Desert. However,

transplanting of these species may be feasible only where a

few plants are needed (McMillan 1960). Although there is a

high risk of seeding failures on areas with low rainfall, range

seeding by transplanting browse species continues to be a

future alternative for the restoration of deteriorated Sonoran

Desert rangelands.

Good brush and grass cover along with an adequate food

source is required to enhance masked bobwhite population

recovery (Guthery 1986). Bobwhite habitat conditions are

good to excellent on the pasture where browse species were

planted. Although the pasture has been protected from

cattle grazing during 2 years and has been grazed light to

moderate for 2 consecutive years thereafter, no quail has

been detected after call counts. Bobwhite possibly already

inhabit the area, but it may be too soon to see big changes in

bird densities after habitat improvement.

Densities of Sonoran mule deer have certainly increased

on brush reseeded pastures. Mule deer numbers have almost doubled since 1996 after planting. Densities of deer

were 1.0 per every 25 ± 4.5 hectares inside the shrub-seeded

pasture and 1.0 per every 48 ± 5.9 hectares in the neighboring pastures. Browse species planted in this pasture have

been found to be an important component of Sonoran mule

deer diets (Ibarra and Martin 1995), consequently, this

range practice will aid in deer habitat improvement and

recovery.

Shredding for Brittlebush Control

in Buffelgrass Pastures

Brittlebush was not significantly reduced by shredding

and densities declined by 12.2 ± 3.5 percent among pastures.

Brush canopy cover was always greater on the control plots

as compared to shredded areas during the study period.

Brush cover was 8.2 ± 1.9 percent after shredding, and 22.3

± 3.5 percent in the three growing seasons after treatment

application. Buffelgrass density averaged 1.9 ± 0.2 p/m2 on

untreated checks and 3.9 ± 0.3 p/m2 on shredded areas in

the three growing seasons after treatment .

Buffelgrass basal cover was consistently greater during

all years on shredded plots. Grass cover averaged 5.2 ± 0.6

percent on untreated control plots and 13.0 ± 1.3 percent on

shredded areas in the three growing seasons after shredding. Forage production of buffelgrass was greater on

shredded plots during all years as compared to untreated

controls. Forage production on shredded pastures varied

from 1.9 to 2.7 ton/ha after the first growing season; from 3.5 to

4.1 ton/ha after the second summer growing season, and

averaged 4.5 ton/ha after the third growing season. Cumulative forage production after three summer growing seasons on shredded stands was 7.82 ton/ha greater as compared to untreated plots.

Although mortality of brittlebush from shredding was low

(8.7 to 15.7 percent) among pastures, top removal temporarily

reduced brush canopy cover (Vallentine 1971). Brittlebush

cover was reduced by 82 percent after shredding, but the

species replaced 48 percent of its original cover three summer growing seasons after shredding. Similar results had

been reported with these and other brush species in Mexico

and Texas (Wright and Stinson 1970; Ibarra and others

1986). However, the rate of replacement of top growth is

variable among species (Reynolds and others 1992), and

depends directly on rainfall after shredding (Scifres 1980).

Consequently, a faster rate of recovery on brittlebush may

be expected when shredding is followed by years of above

average precipitation.

In this study, recovery of buffelgrass stands after shredding may be attributed to temporary brush suppression and

resulting plant competition reduction (Scifres 1980; Bovey

and others 1986). The addition of plant debris to the soil

surface after shredding may also protect the soil from erosion, reduce runoff, increase water availability, and add

organic matter (Vallentine 1991); afterwards, oxidation of

organic matter releases nutrients to the soil for plant use

(Kononova 1968). The establishment of new grass seedlings

was possibly enhanced by soil disturbance caused by

branches, sticks, and shredding blades hitting the soil surface. Results suggest that shredding is an effective range

improvement practice to restore productivity in buffelgrass

pastures highly infested with brittlebush in the Sonoran

Desert.

Although pastures have been rested from grazing during

the year of shredding and they have been light to moderately

grazed thereafter, it is uncertain if masked bobwhite densities have increased on treated pastures. No birds have been

recorded after count calling, despite rancher cowboy reports

that they have seen more birds in the area. Hopefully,

habitat for quail has improved because brush cover of all

other desirable brush and tree species were protected during

shredding. Good brush cover is reported to improve habitat

for bobwhite quail (Guthery 1986). Densities of mule deer

have been consistently greater on shredded pastures as

compared to untreated pastures. Deer counting during the

fall of three consecutive years show 35 to 57 percent more

deer, mainly does, in shredded pastures. The presence of

more succulent forage of grasses and shrubs may account for

deer population increases after shredding (Scifres 1980).

This information suggests that habitat improvement of

deteriorated buffelgrass pastures by shredding may play an

important role in increasing mule deer populations.

Improving Native Rangelands Infested

With Brush by Disk Harrowing

Precipitation at Rancho El Carrizo, Sonora, was close to

the long-term average (325 mm) from 1994 to 1999, except

for 1998 when only 203 mm of rainfall occurred. Total

precipitation at the study site was adequate in quantity and

distribution to promote significant vegetational changes

after disking. Less than 30 percent of the catclaw mimosa

and creosotebush plants were killed by disk harrowing.

Plants that survived disking sprouted vigorously from the

base and reached original sizes within 3 years of treatment

application. Soil disturbance significantly increased density

and cover of most grass and forbs species present in the site

before disking. Bristlegrass (Setaria spp.), buffelgrass,

sideoats grama [Bouteloua curtipendula (Michx) Torr.], and
360 USDA Forest Service Proceedings RMRS-P-21. 2001

Martín-Rivera, Ibarra-Flores, Guthery, Kublesky, Camou-Luders, Fimbres-Preciado, and Johnson-Gordon Habitat Improvement for Wildlife in North-Central ...

tanglehead [Heteropogon contortus (L.) Beauv.] were species

not present on the pasture before disking, but were also

substantially increased after soil disturbance. These plants

are reported as an important source of feed in masked

bobwhite diets (Guthery 1986). Forage production on disked

pastures varied from 750 to 1,100 kg per hectare and was two

to threefold as compared to untreated pastures.

Sonoran mule deer populations were consistently greater

during all years on disking improved pastures. Deer count

estimations indicate that deer numbers were 40 to 65 percent greater in improved pastures as compared to adjacent

untreated pastures. Greater forage availability and richer

species diversity may be attracting more deer to feed inside

the improved pastures. Density of mule deer has varied

among years from 28 to 33 hectares per deer in disked

pastures and from 45 to 51 hectares per deer on untreated

adjacent pastures.

Call counts of masked bobwhite quail show that bird

densities have at least doubled on disked pastures. Ranchers

have reported seeing more birds on the area. Additionally,

bobwhites have been recording even in areas where they

were not found before. There is no doubt that habitat for

masked bobwhite is improved after disking because cover of

desirable brush and tree species were protected during

treatment. Additionally, disking drastically increased some

plants preferred by quail (Guthery 1986). The results of this

study show that selective brush control by disking is an

important habitat management tool for the recovery of

masked bobwhite populations in the Sonoran Desert.

Adopting Grazing Systems for Habitat

Improvement

The short-duration grazing system recently adopted in el

Carrizo ranch in pastures previously rehabilitated by disking

is significantly improving vegetation, cattle performance,

and wildlife recovery. Combination of selective brush competition reduction, soil disturbance, forage production increase, and the control of animal grazing have resulted in

greater ecological and economical benefits. Actual carrying

capacity on treated pastures is at least two to threefold as

compared to untreated pastures. Smaller pastures are facilitating the management of animals. The calf crop has been

increased from 15 to 20 percent as compared to previous

yearly records. Although animal gains are similar in continuous grazing, the number of animals in SDG almost

doubled, despite the established forage utilization of 60

percent or less.

Densities of Sonoran mule deer have almost doubled

within the SDG. Moderate to light grazing is possibly

attracting more deer, as more nutritious feed remains

available in the pastures. Masked bobwhite habitat conditions are good to excellent according to wildlife biologists

throughout the SDG. Grazing is permitted in the system

when cattle can graze forage without damaging masked

bobwhite habitat. Controlling grazing intensity should

improve herbaceous cover conditions and masked bobwhites will have more chances to colonize new areas within

the pasture. Good grazing management is expected to yield

improved habitat conditions for quail.

References _____________________

Benson, L., R.A. Darrow. 1981. Trees and shrubs of the southwestern deserts. University of Arizona Press. Tucson, AZ. 416 p.

Bovey, B.W., Meyer, R.E., Merkle M.G., and E.C. Bashaw. 1986.

Effect of herbicides and hand weeding on establishment of

kleingrass and buffelgrass. Journal of Range Management,

39:547–551.

Canfield, R.H. 1941. Application of the line interception method in

sampling range vegetation. Journal of Forestry, 39:388–394.

Guthery, F.S. 1986. Beef brush and bobwhites. Quail management

in cattle country. Golden Banner Press, Inc. 182 p.

Ibarra, F.A., Martin, M.H., Miranda H., and J.L. Luna. 1996.

Seeding of forage brush species for the restoration of deteriorated

rangelands in the Sonoran Desert. Abstracts 51st Annual Meeting. Society for Range Management. Guadalajara, Jalisco, Mexico.

63 p.

Ibarra, F.A., Martin, H.M., Torres L.R., Silva M.F., Morton H.L.,

and J.R. Cox. 1986. The brittlebush problem and potential control

measures in buffelgrass pastures in Sonora, Mexico. Proceedings

of the Western Society of Weed Science, 39:57–66.

Ibarra, F.F.A. and M.R. Martin. 1995. Establecimiento del Zacate

Buffel. Guia Practica para el Establecimiento, Manejo y Utilizacion

del Zacate Buffel (Eds. PATROCIPES A. C.), Patronato del Centro

de Investigaciones Pecuarias del Estado de Sonora: 15–30.

Kononova, M.M. 1968. Transformations of organic matter and their

relation to soil fertility. Soviet Soil Science, 2:1047–1055.

Martin-R.M., Cox, J.R., Alston, D.G., and F. Ibarra-F. 1995. Spittlebug (Homoptera: Cercopidae) life cycle on buffelgrass in Northwestern Mexico. Annals of the Entomological Society of America,

88:471–478.

McMillan, I.I. 1960. Propagation of quail brush (saltbush). California Fish and Game, 46, 507–509.

Reynolds, J.P., Fulbright, T.E., and S.L. Beasom. 1992. Mechanical

rejuvenation to dampen seasonal variation in chemical composition of browse. Journal of Range Management, 45:589–592.

Scifres, C.J. 1980. Brush management—principles and practices for

Texas and Southwest. Texas A&M University. 360 p.

Shreve, F., and A.L. Hinckley. 1937. Thirty years of change in desert

vegetation. Ecology, 18:463-478.

Springfield, H.W. 1970. Germination and establishment of fourwing

saltbush in the Southwest. Res. Pap. RM-55. Fort Collins, CO:

U.S. Department of Agriculture, Forest Service, Rocky Mountain

Forest and Range Experiment Station. 46 p.

Ueckert, D.N., Petersen, J.L., McFarland, M.L., and R.L. Potter.

1982. Fourwing saltbush revegetation trials in west Texas. Brush

Management and Range Improvement Research 1980-81. College Station, TX. CPR 3968–4014.

Vallentine, J.F. 1971. Range Development and Improvements.

Brigham Young University Press. Provo, UT. 545 p.

Whisenant, S.G., Ueckert, J.L., and J.E. Huston. 1982. Forage

shrub revegetation trial in West Central Texas. Brush Management and Range Improvement Research 1980–81. College Station, TX. CPR 3968–4014.

Wright, H.A., and K.J. Stinson. 1970. Response of mezquite to season

of top removal. Journal of Range Management, 23:127–128.
USDA Forest Service Proceedings RMRS-P-21. 2001 7

Field Trip

361

USDA Forest Service Proceedings RMRS-P-21. 2001 363

In: McArthur, E. Durant; Fairbanks, Daniel J., comps. 2001. Shrubland

ecosystem genetics and biodiversity: proceedings; 2000 June 13–15; Provo,

UT. Proc. RMRS-P-21. Ogden, UT: U.S. Department of Agriculture, Forest

Service, Rocky Mountain Research Station.

Howard C. Stutz is Professor Emeritus, Department of Botany and

Range Science, Brigham Young University, Provo, UT 84602.

Abstract—The field trip was held on June 14, 2000, in warm, dry

weather. It consisted of eleven stops and additional views from the

busses. Many saltbush (Atriplex) species were observed and their

genetical and ecological characteristics described. In addition other

chenopod shrubs and annual chenopods were observed and characterized. The field trip is described so that is can be experienced by

interested parties on subsequent trips.

Introduction ____________________

Much of the Colorado Plateau is occupied by plants in the

family Chenopodiaceae. Almost no other kind of plants can

tolerate the severe challenge of the salty, alkaline deserts

that make up much of the terrain in the Colorado Plateau.

Within the family, the genus Atriplex is by far the most

common, often occupying vast acreages containing nothing

else. Hopefully this tour will serve to introduce a number of

Chenopod species and to portray the ongoing evolutionary

process that is conspicuous at some of the frontiers.

Stop #1: Carbonville, Carbon County, UT; Atriplex

cuneata and A. confertifolia.

Along the railroad embankment are two of the most

common species of Atriplex in the Colorado Plateau: A.

cuneata and A. confertifolia.

1. Atriplex cuneata (“Castle Valley Clover”) is found only

in the Colorado Plateau. The common name of this species

says a lot about its reputation. Its value as an important

forage plant for livestock and other herbivores is derived

partly from its high nutritive potential but probably more

from its occurrence in landscapes that would be completely

empty were it not present.

The distinctive morphological features that distinguish it

from other species of Atriplex are its low, bushy habit, taproot system, burry fruiting bracts, cuneate leaves and early

flowering habit (May). It is mostly dioecious but a few

monoecious plants are usually present in most populations.

Genetically, it occurs at two chromosome levels: diploids

(2n = 18) and tetraploids (2n = 36).

Tetraploid A. cuneata is widespread throughout the Colorado Plateau and is morphologically highly variable. Some of

the variation may be due to phenotypic plasticity in response

to variable environments but most of it appears to be genetic.

Colorado Plateau Chenopod Field Trip

Howard C. Stutz

Some tetraploid forms appear to be direct autoploid derivatives from diploids, others appear to be stabilized segregants

from hybrids, and others appear to be products of introgression. Some isolated populations may have acquired their

uniqueness from new mutations. There are several distinct

forms of diploid cuneata throughout the Colorado Plateau.

Each is phenotypically distinct and each is restricted to a

specific ecological niche.

2. Atriplex confertifolia (shadscale) is distinguished from

all other saltbushes by its broad obtuse leaves, thorny

branches, and two-lipped, unappendaged fruiting bracts.

It is widespread throughout Western United States from

northern Montana to northern Arizona and New Mexico

and from central Colorado to south-central California. On

the Colorado Plateau it occurs as diploids (2n = 18),

tetraploids (2n = 36), and hexaploids (2n = 54). Elsewhere

(Utah, Nevada, Oregon) there are octoploids (2n = 72) and

decaploids (2n = 90).

Diploid shadscale, on the Colorado Plateau, is most

common in rocky soils, often in association with Utah

Juniper. It usually occurs in small, isolated populations in

which between-plant variation is conspicuous. In contrast,

tetraploid populations are usually much larger and show

minimal between-plant variation, suggesting that the

tetraploids are autopolyploid derivatives from single or few

diploid progenitors.

Interspecific hybrids occur, occasionally, between Atriplex

confertifolia and A. canescens, A. corrugata, A. cuneata, and

A. garrettii but no successful product from any of them has

yet been found.

The hybrids between A. cuneata and A. confertifolia as

seen here are fairly common where ever these two species

meet. Notice that the fruiting bracts of the hybrids have two

entire apical lips like those of A. confertifolia and numerous

basal appendages as in A. cuneata. Most hybrid plants are

somewhat thorny, like A. confertifolia.

Stop #2: Wellington, Carbon County, UT; Atriplex tridentata, A. utahensis, A. confertifolia, A.

cuneata, A. powellii, A. corrugata, occasional

Atriplex hybrids, Sarcobatus vermiculatus,

Kochia scoparia, and Sueda torreyana.

About 1 mile south of Wellington, a jumble of ecological

sites brings together several species of Atriplex. In the wet,

alkaline bottoms, there are extensive patches of A. tridentata, salt sage. In contrast to all other species of Atriplex

on the Colorado Plateau, A. tridentata shows extensive rootsprouting. Some individual plants may extend, by root

sprouts, to several meters. Because it is a dioecious species,

the limits of individual plants are usually clearly

discernable. Throughout its geographic range it is highly

variable, probably because it hybridizes with most of the

other Atriplex species that it contacts. Hybrids of A. tridentata with A. canescens are particularly common and, from
364 USDA Forest Service Proceedings RMRS-P-21. 2001

Stutz Colorado Plateau Chenopod Field Trip

these hybrids, have come several new taxa (A. nuttallii,

A. robusta, A. anomala).

On the clay slopes above the populations of A. tridentata

occurs a mixture of chenopods including A. confertifolia,

A. cuneata, A. corrugata, A. utahensis, A. powellii, Kochia

scoparia, Sueda torreyana, and Halogeton glomeratus.

Atriplex “utahensis” is a distinct perennial diploid species

endemic to the Colorado Plateau, mostly in east-central

Utah. It is distinguished by its narrow leaves, upright habit,

tap-root system, and prominent central beak on the copiously appendaged fruiting bracts.

Atriplex corrugata (mat saltbush) is tetraploid in this area

but occurs as a diploid on vast acreages south of here (see

Stops 8 and 9). A. corrugata occupies some of the most severe

habitats found anywhere, often as near monocultures. When

populations collapse, as they have been seen to do during

severe extended droughts, no species other than A. corrugata,

come into the vacant sites. Because of its low stature it is of

minimal value as a forage plant for livestock but is of high

value as a soil stabilizer and habitat for small animals. A.

corrugata plants are easily distinguished by their small,

compact habit, grey color, tiny (3 to 5 mm) linear to oblong

leaves, and two-lipped bracts that are burry below.

Stop #3: East side of Wellington; Sarcobatus vermiculatus.

Sarcobatus vermiculatus (greasewood) is common in alkaline bottomlands in all of the Western States of North

America. Although mostly octoploid (2n = 72) there is considerable between-population variability. Because nurserygrown plants maintain many of their differing, distinguishing features, much of the variation appears to be controlled

genetically. Tetraploid populations of S. vermiculatus are

confined to southern Alberta, southern Saskatchewan, northern Montana, northern California, northwestern Sonora,

Mexico, and southern Arizona and may be relic ancestors to

the more common, widespread octoploid populations. The

genetic variation present among the octoploids may be an

indication of polyphyletic origins or/and subsequent

introgessive hybridization.

Stop #4: Southeast of Sunnyside, Carbon County, UT;

Atriplex canescens var. “cunescens.”

This stop is in a population of Atriplex canescens (fourwing

saltbush) that appears to be introgressed with genes from A.

cuneata.

Atriplex canescens (Pursh.) Nutt. is the most widespread

species of perennial Atriplex in North America, distributed

from southern San Luis Potosi, Mexico, to southern Alberta

and Saskatchewan, Canada, and from the Pacific Coast of

California and Baja California to Texas, Oklahoma, Nebraska, Kansas, and the Dakotas. Throughout its distributional range, A. canescens shows considerable betweenpopulation variation. Some of this variation may be due to

phenotypic plasticity but most of it appears to be genetic.

Mutations, polyploidy, introgressive hybridization, and segregation from interspecific hybrids all appear to have contributed to its extensive heritable variation. Polyploidy is

unusually common with seven identified chromosome races

(2x, 4x, 6x, 8x, 10x, 12x, 20x). A. canescens is also the most

promiscuous of all species of Atriplex and natural hybrids

have been found between it and almost all other perennial

Atriplex species including A. acanthocarpa, A. confertifolia,

A. corrugata, A. cuneata, A. falcata, A. gardneri, A. lentiformis,

A. linearis, A. obovata, A. polycarpa, and A. tridentata.

Many of the hybrids show some fertility and some appear

to have been the source of new taxa. Seed from this tetraploid

population has been valuable in reclamation efforts on BHP

mine spoils in New Mexico.

Stop #5: Bottom lands south of the Carbon-Emery County

line; Atriplex tridentata var. “minutifolia.”

This extensive population of low-statured, small-leaved,

tridentata-like plants appear to have been derived from

hybrids between A. tridentata and A. corrugata. As with

most other tridentata plants, these are hexaploid (2n = 54).

The corrugata plants here are tetraploid (2n = 36).

As you travel south notice the extensive populations of

this still unnamed species on both sides of the road.

Stop #6: Horse Canyon, Emery County, UT; diploid A.

confertifolia (shadscale) and Ceratoides lanata

(winterfat).

The A. confertifolia plants to the south of the exit road

are diploid (2n = 18). The plants to the west are all

tetraploid (2n = 36). Throughout the Intermountain West,

most populations of A. confertifolia are tetraploid. Diploids

are routinely on well-drained upland sites. Two hexaploid

(2n = 54) populations have been found on the Colorado

Plateau, one about 5 miles north of Green River, Utah, and

one south of Cortez, Colorado. Both appear to be allopolyploids derived from hybridization between A. confertifolia

and A. corrugata. Elsewhere, some A. confertifolia occurs

as octoploids (2n = –72) and some as decaploids (2n = 90).

Ceratoides lanata(winterfat) appears to be diploid throughout its wide distribution and shows abundant variation

between populations. Some populations consist of plants

that are less than 6 inches (15 cm) tall. In other populations the plants grow to more than 1 m.

This species is highly prized for its forage value and in

many areas has proven to be valuable in reclamation of

disturbed lands.

Stop #7: Approximately 6 miles west of Green River,

Emery County, UT.

Just before arriving at highway I-70, turn right (west) on

a well-improved road. Continue west for about 1 mile where

there is an extensive mixed population of Atriplex cuneata

and A. corrugata. Interspecific hybridization between them

appears to be common here and many odd-ball segregants

are produced. These species often hybridize in such ecologically “hybrid” habitats and may be responsible for some of

the variation seen in both species.

Stop #8: Green River, Carbon County, UT; annual Atriplex

species: Atriplex minuticarpa, A powellii, and

A. rydbergii.

Most annual species of Atriplex have narrowly limited

distributions, occupy severely restricted ecological sites and

are, within species, morphologically highly uniform. Atriplex

powellii is the principal exception. It is widely distributed,

occupies many different sites, and is morphologically variable, both within and between populations. The reason for

this significant difference appears to be due to its sexuality.

It is the only native annual Atriplex, that is dioecious; all
USDA Forest Service Proceedings RMRS-P-21. 2001 365

Colorado Plateau Chenopod Field Trip Stutz

others are monoecious. Because of its dioecy it is obliged to

outcross whereas monoecious annuals are perpetually inbred, leading quickly to genetic homozygosity.

A. powellii plants are easily distinguished from those of all

other annual Atriplex species. In addition to being dioecious,

the leaves are prominently three-veined and the fruiting

bracts have crown-shaped, two-lipped apices and numerous

basal appendages.

Atriplex minuticarpa, a recently, newly described annual

species is found only on Tununck shale in eastern Utah. It has

previously been confused with A. powellii but here, where

they grow together, they are clearly distinct. A. minuticarpa

is monoecious, A. powellii is dioecious; leaves of minuticarpa

are single-veined, those of powellii are prominently threeveined, and A. minuticarpais smaller statured with divaricate

branching. The severe restriction of A. minuticarpa to a

single, small, geologic formation suggests an ancient origin.

A. rydbergii is restricted in distribution to eastern Utah,

northern New Mexico, and northern Arizona. It usually

occurs in small isolated populations but in some places in

Industrial Valley and near Bluff, San Juan, County, UT,

there are several extensive populations.

Stop #9: 3 miles east of Green River, Grand County, UT;

diploid A. corrugata.

All of these small plants that cover these hills are diploid

(2n = 18) A. corrugata. They differ in phenotype from the

tetraploids in being smaller and more erect. Following

severe drought years it looks like every plant has died.

Subsequently nothing comes back into the vacated acreage

except more diploid A. corrugata. What appears to be an

occasional tetraploid A. corrugata plant is present in the

draws but on the more severe slopes only the diploids

survive.

Stop (pause) #10: 10 miles west of Green River on both

sides of I-70; more diploid A. corrugata.

There is no place to stop here but as we drive along the

freeway, observe the vast populations of diploid A. corrugata

on both sides of the highway. They extend for miles and miles

and miles. What a forest this would be if they could grow up

to be trees.

Stop #11: Hanksville exit from I-70; Zuckia arizonica

and Atriplex saccaria.

Turn north on the dirt road for about mile. Zuckia arizonica

and Atriplex cuneata are common here. Zuckia arizonica

occurs periodically throughout eastern Utah and is very

abundant in northern Arizona, particularly in the Painted

Desert area south and west of Tuba City, Coconino County.

It is a very distinctive species with yellow-green leaves,

brittle branches, non-Kranz leaf anatomy, and six-pointed

fruiting bracts enclosing a horizontally positioned embryo.

Also, here is a distinctive Atriplex annual, A. saccaria. Its

broad, yellow-green leaves are covered with glistening

persistent trichomes that gives the leaf surface a sandpaper appearance. This and A. asterocarpa and A.

graciliflora are the only species with such trichomes. Most

of the fruiting bracts are covered with flattened appendages, a few are small, wedge-shaped, without appendages.

As we return to Provo, watch for the vast populations of

the chenopod species that you now know. This is truly

Chenopod Country! Where there are alkaline, clay slopes

devoid of vegetation, “only” chenopods are encroaching at

these evolutionary frontiers. If and when new species occupy

these empty sites, they will almost certainly be chenopods.

Acknowledgments ______________

Daniel Fairbanks, Durant McArthur, and especially

Stewart Sanderson assisted with the field trip preparation

and discussion.

Contrasts in Utah’s Great Basin and

Colorado Plateau Salt-Desert

Vegetation _____________________

Western Salt Desert Eastern Salt Desert

(Great Basin) (Colorado River Drainage)

1. Many polyploids Few

2. Few diploids Many

3. Low predictability of species by

 ecological site High

4. Low predictability of ecological

 site by inhabitant species High

5. Few well-defined endemics Many

6. Few families, genera, species Many

7. Mostly shrubs Many herbaceous

8. Extensive hybrid swarms Rare

9. Minimal plant succession Conspicuous

10. Vast areas of sudden die back Rare

11. Most species wind pollinated Many other

12. High within-plant plasticity Low

13. High within-population diversity Low

14. Many extensive monocultures Few

15. Few endemic annuals Many

Perennial Chenopods in Western

North America __________________

Genus Number of species

Atriplex 30 +

Ceratoides 1

Grayia 1

Kochia 1

Sarcobatus 2

Suaeda 2

Zuckia 2

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