United States

Department

of Agriculture

Forest Service

Rocky Mountain

Research Station

General Technical

Report RMRS-GTR-14

August 1998

Plant-Herbivore Interactions

in Atriplex: Current State of

Knowledge

Andrés F. Cibils

David M. Swift

E. Durant McArthur
Rocky Mountain Research Station

324 25th Street

Ogden, UT 84401

The Authors

Andrés F. Cibils has the degrees of Ingeniero Zootecnista

(1984) from the Universidad Nacional de Lomas de

Zamora in Buenos Aires, Argentina, and Master of Science in rangeland ecosystem science (1996) from Colorado State University. He is now a Ph.D. candidate at

Colorado State University, working on aspects of the

ecology of Atriplex canescens browsed by cattle in northeastern Colorado. He is presently on leave from the

Instituto Nacional de Tecnología Agropecuaria (INTA),

where he holds a research position with the Natural

Resources Team of the Estación Experimental

Agropecuaria Santa Cruz, Río Gallegos, Santa Cruz,

Argentina. He previously held the position of

Extensionist, also with INTA, in Puerto Deseado, Santa

Cruz, Argentina.

David M. Swift is a Senior Research Scientist at the

Natural Resource Ecology Laboratory and an Associate

Professor in the Rangeland Ecosystem Science Department, both at Colorado State University. He holds a B.S.

degree from the State University of New York, College of

Forestry, an M.S. degree in forest hydrology, and a Ph.D.

degree in animal sciences, both from Colorado State

University. His research included studies of productivity

and stability of traditional pastoral systems in East Africa,

the ecology and nutrition of wild ruminants in Colorado,

and techniques for measuring and estimating carrying

capacity for wild ungulates. He has a long standing

interest in systems ecology and simulation of biological

systems.

E. Durant McArthur is Project Leader and Research

Geneticist for the Shrubland Biology and Restoration

Work Unit at the Rocky Mountain Research Station’s

Shrub Sciences Laboratory in Provo, UT. His degrees

are from Dixie College, St. George, UT (A.S. in physical

sciences, 1963) and the University of Utah (B.S. in

molecular and genetic biology, 1965; and M.S., 1967,

and Ph.D. Degree, 1970, in plant genetics). He was a

Postdoctoral Research Fellow in agricultural botany for

the Agricultural Research Council of Great Britain at the

University of Leeds during 1970 and 1971. He began his

Forest Service research career at the Great Basin Experimental Range at Ephraim, UT, in 1972. He has been

at the Shrub Sciences Laboratory in Provo, UT, since

1975, and has been Project Leader since 1983. He has

held appointments as adjunct professor of botany and

range science at Brigham Young University since 1976.

Research Summary

The body of literature dealing with the biology of

Atriplex is not only extensive and diverse, but is also

scattered among a large variety of sources. The purpose

of this review on plant-herbivore interactions in Atriplex

(saltbushes) was to gain insight into the ecology of

browsed Atriplex stands. Our emphasis was bringing

together and synthesizing research related to the use of

saltbushes as a browsing resource for ruminants. We

took a broad view of the question and included most of

the available literature relevant to the understanding of

the complexities of saltbush-herbivore interactions.

This review is divided into five sections; the first four

sections are divided into relatively self-contained subsections, allowing ready access to information of interest. At the end of each of these sections is a brief

synthesis of common elements in the literature reviewed

from an animal-plant interaction perspective.

The first section discusses aspects of the physiological

ecology and life history of Atriplex that help to understand

why saltbushes have been used so extensively as a

browse resource and also why the ecology of browsed

stands may not be simple. The second section addresses issues related to the effects of browsing on shrub

fitness, and survival and reproductive behavior of saltbushes subject to herbivory and water stress are its

central topics. How saltbushes defend themselves against

herbivory is dealt with in the third section, with special

emphasis on the literature related to saponins, a carbonbased defense compound, common in saltbushes and

other chenopods. The fourth section discusses the effects that saltbushes have on the herbivores that consume them. Data both supporting and questioning the

longstanding reputation that some saltbushes have enjoyed as excellent forage are reviewed in detail in this

segment. In the fifth section we synthesize the information contained in the previous four sections, pointing out

potential interactions between ploidy level, breeding system, defensive chemistry, and herbivory.

Acknowledgments

While we were in the process of writing this publication

we were able to talk to several of the authors of the papers

we reviewed, and in some instances to visit their research sites. We asked many questions about their

published work, and in every case encountered great

generosity in sharing their information and time. We are

greatly indebted to them for the stimulation and help

they gave us. We also thank Drs. Terrance Booth, Bill

Lauenroth, Dave Steingraeber, Darrell Ueckert, and

Carl Wambolt for their valuable input on earlier versions

of this manuscript.
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Contents

Page

Introduction .............................................................. 1

Aspects of the Physiological Ecology and

Life History of Atriplex ........................................ 2

Environmental Conditions ..................................... 2

Photosynthetic Pathways and Productivity ........... 2

Lifespan, Age Structure, and Patterns of

Survival and Recruitment .................................. 4

Ecotypic Variation and Polyploidy ......................... 5

Breeding Systems and Sex Expression ................ 6

Effects of Browsing on Shrub Fitness ...................... 8

Survival and Reproduction .................................... 8

Browsing and Drought Effects ............................ 10

Differential Browsing of Individuals

Within Populations ........................................... 11

Defensive Chemistry of Atriplex ............................. 12

Defense Theory, Dioecious Plants, and

Atriplex ............................................................. 12

Saponins: Chemical Characteristics and

Mode of Action ................................................. 14

Saponins in Other Chenopodiaceae ................... 17

Nutritive Value of Atriplex as a Forage for

Ruminants ....................................................... 17

Chemical Characteristics and Palatability ........... 17

Performance of Ruminants Fed with

Atriplex Diets ................................................... 20

Metabolic Alterations in Ruminants

Consuming Atriplex ......................................... 21

Possible Management Implications of

Herbivore-Atriplex Interactions ........................... 23

References ............................................................. 24

Appendix: Index of Scientific and Common

Plant Names ....................................................... 30

Page
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This publication reports research involving pesticides. It does not

contain recommendations for their use, nor does it imply that the

uses discussed here have been registered. All uses of pesticides

must be registered by appropriate State and/or Federal agencies

before they can be recommended.

CAUTION: Pesticides can be injurious to humans, domestic

animals, desirable plants, and fish or other wildlife—if they are

not handled or applied properly. Use all pesticides selectively

and carefully. Follow recommended practices for the disposal of

surplus pesticides and pesticide containers.
USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998 1

Introduction ____________________

Saltbushes (Atriplex spp.) exhibit a series of outstanding features—such as drought-hardiness, ability to grow in saline and disturbed environments,

and tolerance to metal toxicity—that allow them to

occupy a wide ecological range, spreading from approximately 20 to 50 degrees latitude in both hemispheres. Over 400 species of Atriplex have been identified on six continents, and even though they are

formally considered to be absent from the tropics, a

small number of species have been reported in Central

America and the Caribbean (Le Houérou 1992; Osmond

and others 1980).

The genus Atriplex is among the largest genera of

the Chenopodiaceae. Only Chenopodium challenges

Atriplex in number of taxa (McArthur and Sanderson

1984; Willis and Airy-Shaw 1973). The genus includes

both herbaceous and woody forms. The shrubby taxa

are thought to be more phylogenetically advanced.

Evidence for this is threefold: (1) anomalous secondary thickening of woody stems and roots (Stebbins

1974); (2) C4 photosynthesis is found in many shrubs

but only in a few herbs (Osmond and others 1980); and

(3) many of the shrubs have complicated derived

sexual systems (Maywald 1996; McArthur 1977, 1989;

Parr-Smith and Calder 1979). Atriplex and other

chenopod genera have a high incidence of polyploidy

based primarily on a base (x) number of 9 (McArthur

and Sanderson 1984).

As with other members of Chenopodiaceae, the

ability to succeed in ruderal environments makes

saltbushes highly eligible for reclamation of areas

where human activity has caused serious disturbances (Booth 1985; Goodall 1982; Graetz and Howes

1979; McArthur and Sanderson 1984; Sanderson and

Stutz 1994b; Tiedemann and others 1984). In many

parts of the world, several species of Atriplex—mostly

A. nummularia Lindley, A. canescens (Pursh) Nutt.,

and A. halimus L.—have been cultivated extensively

on rangelands degraded through overgrazing, on

saline scalded areas, and on strip-mined lands.

Such seeded stands of Atriplex are often used as a

Plant-Herbivore Interactions

in Atriplex: Current State of

Knowledge

Andrés F. Cibils

David M. Swift

E. Durant McArthur

supplementary forage resource to feed small ruminants during periods of drought. Examples from the

literature point to work carried out in some African

countries (Egypt, Libya, Tunisia, Algeria, Morocco,

Sudan, and South Africa), countries of the Middle East

(Israel, Iraq, Syria, Iran, Yemen Arab Republic, and

Saudi Arabia), Pakistan, Australia, and the United

States (Abdul-Halim 1986; Atiq-ur-Rehman 1990 a,b;

El Hamrouni 1986; Forti 1986; Gihad and El Saher

1992; Hobson and others 1986; Kessler 1990; Khair

1992; Khalil and others 1986; Nemati 1977; Runciman

1986; Sankary and Goodin 1986).

In the livestock industries of many arid and semiarid areas of the world, several species of Atriplex are

considered a valuable browsing resource during

periods of forage scarcity because their foliage is

evergreen and exhibits a fairly high crude protein

content. A large body of work dealing with nutritive

value of Atriplex spp. (mainly A. canescens) and their

potential use as browse for livestock has been published in recent decades (Atiq-ur-Rehman 1990a,b;

Benjamin and others 1992; Benjamin and others 1995;

Bhattacharya 1989; Chatterton and others 1971;

Clarke 1981; Davis 1981; Garza and Fullbright 1988;

Glenn and others 1992; Goodin 1979; Holecheck and

others 1990; Kessler 1990; Khalil and others 1986; Le

Houérou 1992; Leigh 1972; Leigh and Wilson 1970;

McArthur and others 1984; McKell 1989; Nemati

1977; Northington and others 1979; Otsyina and others

1982; Rumbaugh and others 1982; Shoop and others

1985; Silva Colomer and Passera 1990; Sims and

Taylor 1973; Ueckert and others 1990a,b; Warren and

others 1990; Welch and Monsen 1981, 1984; Welch

1989; Weston and others 1969; Wilson 1966a,b, 1977).

The enthusiasm of some authors who have looked

at chemical components of edible saltbush material,

and reported its outstanding nutritional attributes, is

not always shared by others who have carried out

feeding-trial studies. Some of the latter suggested

that under certain circumstances, animals fed on a

diet composed entirely of saltbushes suffered detrimental metabolic alterations. These were probably

caused by the presence of secondary compounds (such
2 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998

as saponins) or nonprotein nitrogenous compounds

(glycinebetaine, for example) that cannot be readily

utilized by ruminal microbes. Le Houérou (1992),

arguing in favor of the nutritional attributes of Atriplex, stated that some of this controversy could be

explained by the fact that feeding trials are generally

too short to allow animals and microbes to adapt to

saltbush diets.

A number of distinctive traits of Atriplex, including

dioecy, female-biased sex ratios, sexual lability, polyploidy, and the presence of defense compounds, can

confer a considerable degree of complexity to plantherbivore dynamics in browsed populations. Browsing

can affect male and female phenotypes differently.

Preferential browsing and crown size reduction of

female individuals can affect female reproductive

fitness and alter sex ratios, in some cases to the

extreme of impairing reproduction in local populations (Freeman and others 1993; Maywald, personal

communication; Williams and others 1978). Secondary compounds could be responsible, in some cases, for

the patterns of differential browsing among individuals of saltbush stands (Otsyina 1983; Sanderson and

others 1987). Higher ploidy level is thought to reduce

palatability to browsers (Stutz 1989), thus allowing

for browsing selection in favor of higher ploidy level

individuals in situations where shrubs of different

ploidy levels coexist. Stress factors such as extremely

cold winters, droughts, or prior heavy seed-set by

females can induce changes in sex expression, generally toward maleness (Freeman and McArthur 1984;

McArthur 1977; Van Epps 1975).

Aspects of the Physiological

Ecology and Life History of

Atriplex ________________________

Environmental Conditions

Most saltbush species prosper in areas with annual rainfall ranging from 200 to 400 mm. Where

average precipitation is less than 200 mm, certain

Atriplex must either behave as phreatophytes or receive irrigation in order to survive (Le Houérou 1992).

Above 200 mm of yearly rainfall, this genus has adapted

to a very broad range of temperatures—from cold

coastal environments of northern Europe to very

hot desert habitats such as Death Valley in California

(Osmond and others 1980). According to Le Houérou

(1992, p. 118), arid land saltbushes “...may be considered among the most heat-tolerant terrestrial

dicotyledons.” Cold temperature resistance, on the

other hand, varies among and within species of this

genus. Le Houérou (1992) divided Atriplex into

three groups based on tolerance to cold temperatures:

1. A cold-resistant group, comprising several species

that grow in the Great Basin of the United States, are

known to withstand temperatures as low as –20 °C;

some ecotypes of A. canescens are among them. Walser

and others (1990) reported that in the Intermountain

West, A. canescens did not reach lethal cold temperature until –80 °C in the winter, and that buds withstood temperatures of up to –35 °C in the spring.

2. Species such as A. padulosa, A. barclayana, and

the Chilean A. repanda are known to be cold sensitive.

Exposure to extended periods of –5 °C could be lethal

to species of this group.

3. The Australian A. vesicaria Heward ex. Benth.

and A. nummularia, together with the Argentinean

A. lampa and some ecotypes of the North American

A. canescens, are included in an intermediate group,

withstanding moderately tolerant to cold temperatures.

There are some remarkable examples of drought

resistance among Atriplex, such as Atriplex hymenelytra, that have survived 10 days at –6MPa of water

potential in the root zone (Clark and others 1974).

However, extensive shrub die-offs, especially of A. confertifolia (30 percent mortality in upland sites in

western Utah due to a severe drought in 1931) (Stewart

and others 1940), have been reported in the Great

Basin as a consequence of environmental stresses

such as drought, winter injury, or excessive rains

(Nelson and others 1989). Le Houérou (1992) pointed

to the fact that tolerance to drought and salinity was

variable among species of Atriplex. He proposed a

classification of species on the basis of salt and water

stress resistance that ranges from the Xerohypohalophytes to the Hygro-hyperhalophites. The former

included species such as A. glauca, A. semibaccata,

and A. leucoclada, able to endure conditions of very

low moisture and low salinity; and the latter comprised species such as A. coriacea and A. barclayana,

unable to endure conditions of low moisture but successful in highly saline environments.

Low temperature is probably one of the few abiotic

factors that limits the spread of this genus. However,

the extraordinary range of environmental conditions

in which members of Atriplex are successful points to

their capability to respond to abiotic selective forces

and to adapt to extremely dissimilar local conditions.

Intraspecific variation, a characteristic of most members of the genus, is critical to their ability to adapt to

contrasting environments.

Photosynthetic Pathways and Productivity

Contrary to what has been observed in most shrubs,

the C4 carboxylation pathway is present in the

majority of Atriplex species. A few cases exhibiting

the C3 photosynthetic pathway, generally living in

colder and more mesic environments and exhibiting
USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998 3

herbaceous growth habit, have also been reported

(Osmond and others 1980).

Laboratory experiments measuring gas exchange,

photosynthesis, and water use efficiency of leaves

and whole plants of C3 and C4 Atriplex found higher

water use efficiency and productivity in the C4 specimens (Slayter 1970). Transplant experiments with

A. patula (C3) and A. rosea (C4) in northern California

suggested that C3 species were better adapted in

moister coastal environments, while C4 species seemed

to be at a competitive advantage in dry desert habitats

(Björkman and others 1969; Nobs and others 1972).

Transpiration and uptake of a soil-applied insecticide

([14C]phorate) in a greenhouse experiment showed

higher transpiration and insecticide uptake rates in

the C3 A. patula compared with the C4 A. rosea

(Anderegg and Lichtenstein 1981). Greenhouse experiments conducted by Dwyer and DeGarmo (1970)

in New Mexico, measuring root and shoot production,

and water use efficiency of three native C3 shrubs

(Larrea tridentata [D.C.] Coville, Prosopis juliflora

[Swartz] D.C., and Gutierrezia sarothrae [Pursh] Britt.

and Rusby), and the C4 A. canescens, found the

latter to be the most efficient in the use of water and

on average the most productive. However, in cold, dry

environments where C3 and C4 chenopod shrubs coexist, studies at the plant community level have not

demonstrated clear advantages of one pathway over

the other in terms of total (above and below ground)

primary productivity measured throughout a growing

season (Caldwell 1974; Caldwell and others 1977).

Results from research in Australia suggest that

some Atriplex are able to perform as well or better

than agronomic species exhibiting either the C3 or C4

photosynthetic pathway when water and nutrient

supplies are not limiting (Osmond and others 1980).

Jones and others (1970) grew two species of Atriplex

(A. nummularia and A. vesicaria), a native cool season

grass (Danthonia caespitosa), and common sunflower

(Helianthus annuus) under controlled radiation and

temperature conditions. Their data showed greater

productivity performance in A. vesicaria compared to

the other species, including the C3 H. annuus. They

also measured photosynthesis of field-grown A. nummularia (C4) and Zea mays (C4), and found that even

though Z. mays exhibited greater maximum leaf photosynthetic rates, whole plant photosynthetic rates

were higher in A. nummularia.

Many researchers have measured and reported primary productivity values for several Atriplex under

different environmental conditions. Aboveground productivity values for both native and cultivated saltbush stands range from 12 to over 700 g per square m

per year (Correal 1983; Gittens 1995; Goodin 1979;

Liang and others 1989; Otsyina and others 1982;

Passera 1983; Petersen and others 1987; Rumbaugh

and others 1982). Productivity reported by these

authors is in many cases hard to compare because

of differences in the methods used and incomplete

information on shrub densities and soils. Le Houérou

(1992) stated that rain-use efficiency in well-managed,

cultivated stands of A. nummularia, A. halimus,

and A. canescens in the Mediterranean area ranged

from 5 to 10 kg aboveground dry matter per ha per year

per mm of rain.

Differences in photosynthate allocation within species exhibiting the C4 pathway result in dissimilar

root:shoot ratios and in potentially different

aboveground productivity values (Osmond and others

1980). These authors quoted research carried out

with Atriplex vesicaria, a warm-desert saltbush, and

A. confertifolia, a cold-desert saltbush, that exhibited

root:shoot ratios of 0.3 and 7.0, respectively. They

pointed to the fact that cold desert Atriplex invested

greater amounts of assimilates in root structure than

warm desert C4 plants of the same genus, in keeping

with an empirical model proposed by Davidson (1969).

This model predicted greater root:shoot ratios as soil

temperatures depart from the optimum; its underlying assumption was that, within a certain range,

increases in temperature triggered root activity increases, thus enabling a plant to invest less assimilate in root structure. The opposite was predicted to

occur when temperatures were lower than the optimum. However, by the same token, an increase in

temperature could promote root growth by favoring

the conversion of assimilates and mineral nutrients

into root structure (Wilson 1988). Probably, the striking differences in cold- and warm-desert C4 Atriplex

root:shoot ratios could be better explained by the

interaction of several factors. Carbon and nitrogen

uptake and translocation, together with moisture availability and both soil and air temperatures, might be

some of the factors interacting to produce the observed

patterns (Cannell and Dewar 1994; Thornley 1976;

Wilson 1988). The idea of other factors, besides temperature, affecting root:shoot ratios is supported by

research on A. litoralis (Steen 1984). He studied root

and shoot growthof plants under different fertilization

and irrigation treatments. He reported lower root:shoot

ratios for Atriplex plants fertilized with K and NPK,

compared with unfertilized plants. He also reported

lower root:shoot ratios for plants irrigated with sea

water, compared to those irrigated with fresh water.

Primary productivity of deserts and semideserts

has been estimated to range from 10 to 250 g dry

weight per square mper year (Whittaker 1975). Longterm data from the Atriplex vesicaria warm-desert

communities of the Koonamore Vegetation Reserve in

Australia showed productivity values that place

these systems among the least productive (aboveground productivity = 26 g per square m per year) of
4 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998

arid land ecosystems (Noble 1977). Conversely, colddesert A. confertifolia communities of the Desert

Experimental Range in Ephraim, UT, USA, are among

the most productive communities of dry systems

(aboveground productivity = 195 g per square m per

year) (Hutchings and Stewart 1953). These findings point to the fact that different species within the

genus Atriplex, exhibiting the same photosynthetic

pathway, have evolved the ability to succeed over a

relatively broad environmental range.

Allocation patterns, photosynthetic pathways, and

productivity of saltbushes are clear examples of both

their enormous genetic variability and phenotypic

plasticity. Many species of the genus are particularly

attractive as a resource for forage production in agricultural systems of marginal areas because of the high

productivity potential conferred by their C4 photosynthetic pathway. The ability of Atriplex to produce

as much or more biomass than traditional forage crops

with irrigation, added to its stress-tolerance features,

explains why Atriplex has been extensively used in

revegetation projects for arid lands.

Lifespan, Age Structure, and Patterns of

Survival and Recruitment

Anomalous secondary thickening, derived from several successive cambia, occurs in woody species of

Chenopodiaceae, Amaranthaceae, and Nyctaginaceae

(Fahn and Zimmermann 1982). Both woody and herbaceous genera of the Chenopodiaceae share this anatomical feature. Woody chenopods are believed to have

arisen from the herbaceous members of the family,

exhibiting an evolutionary trend opposite to what has

usually been described for flowering plants in continental floras, such as herbaceous genera deriving

from the woody genera of a family (McArthur and

Sanderson 1984; Stebbins 1974).

As a member of the Chenopodiaceae, Atriplex exhibits included phloem, an anatomical peculiarity that is

characterized by scattered groups of phloem cells

included within secondary xylem bundles embedded

in a conjunctive parenchyma tissue (Fahn 1974). While

these anatomical modifications may confer resistance

in harsh environments, secondary growth driven by

successive cambial segments (with no real growth

rings present) makes age assessment by means of

vascular ring counts very difficult (Fahn and

Zimmermann 1982). Schweingruber (1992), studying

annual growth rings of native shrubs and trees of

Australia, examined 16 woody species from the

Chenopodiaceae. He reported that he was unable to

determine their ages, partly due to his uncertainty as

to whether the ring-like structures reflected yearly

growth. In A. halimus, faint borders between increments in secondary body have been identified, yet

methods involving labeled carbon might be the only

way to tell if such increments correspond with annual

growth cycles of the shrub (Abraham Fahn, personal

communication).

Most authors who have looked at life spans in species of Atriplex agree in describing them as mediumto short-lived shrubs (but see Gulmon and Mooney

1977). Early research carried out in southwestern

Utah reported counts of up to 40 vascular rings in

A. confertifolia (Stewart and others 1940). Norton

(1978) analyzed data from the Desert Experimental

Range in southwestern Utah, on persistence of grazed

and protected populations of A. confertifolia, for a

40 year period (1935 to 1975). He reported that in

1975, 67 and 77 percent of the grazed and ungrazed

populations, respectively, were made up of plants

that were less than 17 years old. West (1979) analyzed

survival patterns of two cohorts of several cold-desert

shrub species at the same site for a slightly shorter

period (1935 to 1968). He found relatively high mortality in A. confertifolia in the first 2 years after establishment and in the last 10 years (1958 to 1968) of

his analysis. He reported that in 1968, survival of the

individuals of the 1935 cohort was 39 and 36 percent

for grazed and ungrazed plots. Survival curves and

tables (West 1979) suggest half-life “...time taken for

a population to fall by 50 percent” (Harper 1977, p. 553)

of approximately 27 years for this cohort of shadscale.

Crisp (1978), working on demography and survival of

A. vesicaria in the Koonamore Vegetation Reserve in

South Australia, reported a half-life of 11 years for

individuals of the population he studied. Yensen and

Smith (1984) reported a mean age of 24 years (ranging from 3 to 61) for a sample of individuals from a

population of A. falcata in southwestern Idaho. These

authors used vascular ring counts to assess shrub

ages, and pointed to the fact that anomalies in vascular growth patterns, typical of woody chenopods, could

have rendered their results inaccurate.

Age structure assessment of Atriplex populations

can be particularly meaningful to studies of structure

of plant communities and population dynamics, and is

by no means a trivial matter in studies of grazing and

climate effects on saltbush populations. In an analysis

of population pattern in chenopod communities of

southern Australia, Anderson (1967, p. 456) found

age-related alterations in the intensity of patterns

in A. vesicaria “...expressed as the ratio observed/

expected mean square for the appropriate block size.”

Revisited work carried out by Anderson (1967) found

that pattern in A. vesicaria populations was in part

due to “...an age-dependent phenomenon” (Malik and

others 1976, p. 267). Malik and others (1976) stated

that pattern was basically determined by the younger

individuals; analysis of data subsets containing only

older plants found an essentially random distribution.
USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998 5

To avoid problems associated with establishing ages of

individuals, these authors divided the populations

into four age categories (seedling, pioneer, building,

and mature) on the basis of crown diameters.

Survival curve shapes for Atriplex confertifolia cohorts are not constant over time. The negative slope

curve describing constant death rates in the two

cohorts studied by West (1979) best characterized

mortality of plants older than 2 to 3 years of age up to

34 years of age. Mortality rates for younger and older

plants were considerably greater. This author reported no statistical differences in the shapes of mortality curves for grazed and ungrazed situations. However, Chambers and Norton (1993), studying the effects

of grazing and drought on population dynamics of

several grass and shrub species at the same site,

reported higher adult mortality in the heavily grazed

plots compared with the protected areas, irrespective

of grazing season. They conducted their study between

1975 and 1978, a period that included several extremely dry years. They stated that “A. confertifolia

is susceptible to the effects of below-average precipitation and that these effects are exacerbated by grazing” (p. 268). Recruitment of new individuals, on the

other hand, was highest in the plots that had been

most affected by grazing (the heavily grazed spring

plots). These were the only plots to exhibit positive

population turnover rates. Norton (1978) stated that

in 1975 there were three times more shadscale individuals in the heavily grazed pastures, relative to the

exclosures at this same site. Both Norton (1978) and

Chambers and Norton (1993) attributed these differences to interspecific competition; the decrease of

the more palatable species had allowed the less palatable (armed) shadscale to increase. Harper and others

(1990), Kitchen and Hall (1996), and Whisenant and

Wagstaff (1991) also studied shrub dynamics (including shadscale) at this site, using portions of the same

data set analyzed by Chambers and Norton (1993),

Norton (1978), and West (1979). These authors all

concluded that season of grazing had important impacts on shrub dynamics. Shadscale densities were

found to be independent of or even enhanced by grazing under the management practices at the Desert

Experimental Range.

In Atriplex vesicaria, survivorship curves change

over time. Heavy early mortality (type III survival

curve) later changes to constant death rates (type II

survival curve) (Crisp 1978). Crisp (1978) also described this shrub as exhibiting a fairly continuous

recruitment strategy. In research on A. vesicaria

on the Mundi Mundi Plain in New South Wales,

Australia, Eldridge and Westoby (1991) reported 20

recruitment events out of the 21 periods they observed (between 1977 and 1987). They stated that

recruitment occurred in all seasons, and survival of

propagules was independent of the size of the recruitment event. Recruitment was also reported to occur

irrespective of adult shrub density in the areas they

sampled. The authors argued that their data suggested seed supply did not restrict recruitment in

bladder saltbush stands with more than about 1,000

adult shrubs per ha. Contrary to what Crisp (1978)

reported, survival patterns at this site were constant

through time, and drought events affected both adults

and young plants alike. Eldridge and Westoby (1991)

attributed these disparities both to soil dissimilarity

between the Koonamore site and their study area, and

to differences in the length of time through which

cohorts were followed at both sites.

Determining age structures in saltbush populations

appears to be a challenge that has not received full

attention in research dealing with the ecology of Atriplex, probably due to the considerable degree of complexity associated with the issue. Several authors

have used age surrogates that have allowed reasonable approximations to the problem. However, questions about individual plant longevity of a number of

Atriplex species remain unanswered. More accurate

methods for establishing ages of saltbush shrubs

(such as pantographic techniques) would undoubtedly

advance the present understanding of population

processes and patterns in browsed Atriplex stands.

Ecotypic Variation and Polyploidy

Speciation due to intraspecific differentiation and

hybridization is a relatively common phenomenon in

this genus (Le Houérou 1992; Osmond and others

1980; Stutz 1978; Stutz 1989). In fact, the concept of

ecotype, as first developed at the beginning of the

century by Turesson (1922), was in part a result of

research on erect and decumbent growth forms of the

annual Atriplex litoralis.

In North America, Atriplex canescens exhibits a

remarkable dispersion area, occupying sites from

Canada to Mexico, and from the Missouri River to the

coast of the Pacific Ocean (Stutz and others 1975).

Its ability to succeed over such a widespread area is

explained by the degree of phenotypic plasticity it displays (associated with significant morphological variation) and by processes of hybridization and polyploidy

that originate intraspecific heritable variation

(Sanderson and Stutz 1994a; Stutz and Sanderson

1979).

Polyploidy, which is known to occur in numerous

dryland shrubs (Artemisia spp., Chrysothamnus spp.,

Larrea sp.), is present in several species of Atriplex

(McArthur 1989; Stutz 1989). Although only one third

of the known saltbush species have been described as

polyploids, North American saltbushes exhibit this

feature fairly frequently. In populations of A. canescens,
6 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998

autopolyploids are far more abundant than diploids

(Osmond and others 1980; Stutz 1989), and various

authors have ascribed adaptive significance to this

feature, occurring not only in A. canescens but also in

A. confertifolia and A. tridentata (Dunford 1984, 1985;

Sanderson and others 1990; Senock and others 1991;

Stutz and Sanderson 1983; Stutz and others 1975;

Stutz and others 1979).

Dunford (1984, 1985) studied distribution patterns of

cytotypes of Atriplex canescens in southern New Mexico

and northwestern Texas. He found that diploid (2n =

18) plants grew mainly on sandy soils of the mesas,

while hexaploid individuals (2n = 54) could be found

growing on the heavier alluvial soils of the floodplains.

Tetraploids (2n = 36) were present on both soil types.

He explained this distribution pattern as a plant

adaptation to different soil textural types. This pattern confirmed research results of Stutz and his colleagues (Stutz 1989; Stutz and others 1975) who found

a population of diploid plants of A. canescens, which

they described as “...a gigas form of A. canescens,” on

the sandy soils of the Little Sahara Sand Dunes near

Delta, UT. This diploid population grows three to four

times taller than the normal A. canescens of the area.

The area surrounding the sand dunes was inhabited

by tetraploid plants, yet none of these were found

growing on the dunes. Likewise, these authors were

unable to find diploid individuals growing on the finer

textured soils surrounding the dunes. In transplant

gardens, the diploid gigas seedlings have far greater

growth rates compared with “normal plants.” Mature

diploid plants exhibit unusual growth rates of new

twigs, being able to put on as much as 100 cm of growth

in a single growing season. McArthur and others

(1983) found the gigas diploid to be among, yet not

above, the leading producers in an 18-accession comparative study. This study was conducted on clay loam

and stony loam soils. Senock and others (1991) studied

differences in leaf morphology among cytotypes of

A. canescens at a site near Las Cruces, NM. They found

higher water use efficiency in hexaploids and

tetraploids than in the diploid cytotype. Similar ecotypic differences have been reported for A. confertifolia by Stutz (1989), who stated that diploid shadscale

could be found growing above the Pleistocene lake

levels in the Great Basin, while tetraploids were

presently found on the lakesides and various polyploids (4x, 8x, or 10x) in the ancient lake bottoms.

Contrary to what occurs in grasses and other herbaceous plants, increase in chromosome numbers in

many shrub species decreases stature (Stutz 1989).

Stutz observed this pattern among Atriplex canescens

plants and argued that reduced size was of adaptive

importance because it was associated with an increase

in drought tolerance and a decrease in palatability to

browsers. Studies of Artemisia tridentata, A. confertifolia, and Chrysothamnus viscidiflorus reviewed and

augmented by Sanderson and others (1989) tend to

confirm this relationship between ploidy level and

plant size. However, in A. confertifolia, even though

tetraploids are smaller than diploids, octoploids and

hexaploids have similar statures, and decaploids are

larger than both tetraploids and octoploids. These apparent deviations from the observed shrub-size:ploidylevel patterns were attributed to interspecific competition and adaptation to saline environments.

Sanderson and others (1989) also pointed to findings

of Solbrig (1977) in Gutierrezia sarothrae, and Stutz

and others (1987) in Grayia brandegei, where shrub

size increased with ploidy level.

Few authors have addressed questions related to

the ways in which selective forces exerted by browsing

may affect saltbush populations. Genetic processes

that allow Atriplex to adapt to abiotic selective pressures should also confer browsed saltbush populations

the ability to adapt to herbivory. The great variability

and the active differentiation processes previously

described suggest that the probabilities of occurrence

of browsing-adapted saltbush genotypes should be

high. The literature, however, reports more examples

of local extinctions than adaptation to browsing by

large herbivores. Nevertheless, moderately long-term

browsed saltbush stands should offer unique opportunities to answer questions related to adaptations to

browsing.

Breeding Systems and Sex Expression

Breeding systems regulate the flow of genes among

plants. Shrubs, in particular, have evolved many of

these systems that allow them to maintain genetic

variability and succeed in patchy environments

(McArthur 1989). Dioecy is a diclinous breeding system where each genet usually expresses one sex and,

in angiosperms, is thought to have arisen from selfcompatible inbreeders as a response to selective pressure for outbreeding or separation of male and female

function (Richards 1986). Monoecy, on the other hand,

is a monoclinous breeding system where sexual functions are separated in male and female flowers within

the same plant. In this way, monoecious plants are

hermaphroditic, but their flowers are not perfect,

exhibiting either male or female functions (Richards

1986).

The dioecious condition is much less common than

the perfect flower condition in flowering plants. Frequency of dioecy is higher than normal in some

tropical forest woody species and island floras, in

particular those from Hawaii and New Zealand (Bawa

1980). Both these cases and additional evidence from

gymnosperms have been used to postulate models
USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998 7

that explain evolution of dioecy, either as a response

to selective pressure against inbreeding, such as the

case of island floras, or as a result of selective forces

acting through pollination and dispersal ecology of

species, such as the case of tropical forests and gymnosperms (Bawa 1980; Bawa 1982; Givnish 1980; Givnish

1982; Thomson and Barrett 1981). Freeman and others (1980b) quantified the occurrence of dioecy in 40

different plant communities of the Intermountain

West of the United States, ranging from the deserts in

northwestern New Mexico to the alpine meadows of

the Wasatch Mountains. They found the dioecious

habit to be somewhat more frequent in this region

than had been reported for angiosperms as a whole in

the literature. They were also able to find a fairly

strong positive association between dioeciousness and

both anemophily and woody life-forms. These authors

concluded that dioeciousness “...has arisen repeatedly

through disruptive selection processes that are maximally effective in patchy environments dominated by

anemophilous, woody species” (p. 416). In patchy environments, dioecy reduces intraspecific competition

and enhances niche occupation through spatial

segregation of male and female plants along moisture

gradients (Freeman and others 1976, 1997; McArthur

1989).

Baker (1959) stated that most annual Atriplex were

monoecious, while perennial individuals were commonly dioecious. Brown (1956) described dioecy as the

most frequent breeding system in perennial species

of North American Atriplex. Asexual reproduction

has also been reported for A. tridentata (saltsage)

and A. canescens (Nord and others 1969; Stutz 1989;

Woodmansee and Potter 1970).

Breeding systems of tetraploid populations of

Atriplex canescens studied by McArthur and Freeman

(1982) were described as the “trioecious state of

Darwin (1877)” (p. 481). These populations exhibited

three floral phenotypes (males, females, and monecious or hermaphroditic individuals), with a fairly

constant ratio of pistillate:staminate:hermaphroditic

plants, clearly biased towards female sex expression.

McArthur (1977) proposed a theoretical 55:35:10 ratio

of sexual phenotypes, on the basis of a 7 year study he

conducted on sex expression of a half-sib family of

tetraploid A. canescens in a common garden in

Ephraim, UT. Subsequent research conducted by

McArthur and Freeman (1982), comparing 19 natural

tetraploid populations from Utah, New Mexico, Arizona, Montana, Idaho, Oregon, and Colorado, showed

that ratios of 11 out of the 19 populations did not differ

significantly from the proposed ratio (55 pistillate:35

staminate:10 hermaphroditic). Similarly, the pooled

ratio of all 19 populations was not significantly different from the theoretical ratio. In this paper, data from a

diploid population were also reported; sex ratios were

1 pistillate:1 staminate, with no presence of hermaphroditic plants. Barrow (1987) surveyed native

populations of diploid, tetraploid, and hexaploid A.

canescens in southern New Mexico and western Texas

and found ratios similar to those described by McArthur

and Freeman (1982). However, Barrow (1987) reported the presence of a few hermaphroditic individuals in the diploid populations. He found that numbers

of hermaphrodite individuals increased with ploidy

level. A study of four ecotypes of tetraploid A. canescens

from western Texas showed sex ratios similar to those

described above (Petersen and others 1987). Two

ecotypes from more xeric environments exhibited less

staminate plants and more shrubs with no sexual

expression when grown in a common garden together

with the other two ecotypes. Petersen and others

(1987) attributed this to environmental controls of sex

expression. Cibils and others (1997) found similar

ratios in a winter-grazed stand of tetraploid A.

canescens on the shortgrass steppe in northeastern

Colorado. However these authors reported significantly different ratios (more female-biased) in longterm exclosures at the same site.

Stress conditions, defined by Charnov (1982) as

those “...which reduce growth, reduce a plant’s ability

to allocate resources to reproduction, or lessen an

individuals chances for survival” (p. 204), can induce

sex change in some individuals of tetraploid Atriplex

canescens. McArthur (1977) reported this phenomenon

in the half-sib population he studied where 30 percent

of the individuals changed their sexual phenotype

after a mild autumn and extremely harsh winter sequence. Over a longer period, McArthur and Freeman

(1982) reported that 59 percent of the individuals of

this population showed constant sex expression, while

41 percent were sexually labile. They stated that sex

changes were generally towards maleness and that

greatest lability was found among the monoecious

plants. All but one of these plants changed sex over the

6 year study period. Among females, 51 percent changed

sexual expression, this occurred only in 15 percent

of the males. Sex lability in tetraploid populations of

A. canescens is thought to be genetically constrained

(for example, environmental stress factors can induce

sex change only in some individuals). McArthur (1977)

proposed a model to account for this, whereby sexual

genotypes would be either: XXXX, exhibiting a constant female phenotype; XXYY, showing a constant

male phenotype; or XXXY, exhibiting a sexually labile

phenotype. Both X and Y represented either loci or

blocks of loci responsible for the genetic control of

sexual expression. McArthur and others (1992) conducted a long-term (20 year) study using clonal material that demonstrated some individual plants are

fixed in sex expression and others are labile, for example, they can respond to environmental cues by
8 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998

being male, female, and monecious on a temporal

scale. Freeman and others (1993) and McArthur and

others (1992) postulated that this trioecious system is

an adaptation that allows fourwing saltbush individual plants and populations to more effectively occupy patchy heterogeneous habitats.

Freeman and others (1980a) stated that shifts in

sexual expression in plants had been reported in 25

families and over 50 species of flowering plants. In

some cases, changes imply year-to-year variation in

sex expression of individuals, while in others, it occurs

as sequential hermaphroditism driven by plant size.

Moisture stress, severe winters, decreasing light intensity, and removal of reserve organs have all been

reported to produce shifts towards maleness. The

mechanisms responsible for these changes could include induced plant hormone imbalances (gibberellic

acid:cytokinin ratios), especially in the case of water

stress (Freeman and others 1984). Male and female

individuals of some dioecious species are not equally

fit in all environments. Because of this, it has been

suggested that sexual lability could be of adaptive

significance to species growing in patchy environments and a means to maximize population reproductive fitness (Charnov 1982; Freeman and others 1980a;

Freeman and others 1984). In several species of

Atriplex, females were found to be under greater

internal water stress than males when fruit was in

late stages of development or soils were dry (Freeman

and McArthur 1982). This could explain in part the

patterns of spatial segregation of sexes in Atriplex

populations (Freeman and others 1976; Freeman and

others 1993).

Sex ratios can be altered by environmentally induced sex switching. Freeman and McArthur (1984)

studied the relative importance of mortality, nonflowering, and sex lability in biasing sex ratios of natural

populations of Atriplex canescens, A. confertifolia, A. corrugata, and A. cuneata. They found sex change and

nonflowering to be considerably more important

than mortality, even though the relative importance

of each factor changed from year to year. Strawbridge

and others (1997) examined a population of A. amnicola

over 5 years and reported sexual lability. Females and

monoecious shrubs increased over the years, a process

that the authors attributed to aging rather than environmental stimuli. Other factors, such as browsing,

could also be responsible for biasing sex ratios. Williams

and others (1978) reported they found male-biased sex

ratios in a population of A. vesicaria due to preferential browsing of female shrubs by sheep. In this case,

sheep browsing appeared to reduce survival of female

shrubs. Even though browsing may be a factor inducing sex change, reports on this in the literature are

not clear. Maywald (1996) reported that A. vesicaria

includes labile plants in addition to males and females.

Freeman and others (1980a) stated that examples

from their literature search showed that leaf removal

or crown-pruning produced shifts towards femaleness (contrary to the general stress-induced sex shift

trend) in at least eight species of plants. Finally,

competition was also hypothesized to alter sex ratios

in A. confertifolia (Freeman and Harper 1980). At

the site of their study, males were overrepresented

inside protected areas, while females were more abundant outside in the grazed pastures. Freeman and

Harper (1980) postulated that water stress due to

competition was greater inside exclosures. This condition would affect females more negatively than males

and, hence, the bias in ratios they observed. They also

mentioned that, in this armored species, males exhibit

fewer thorns than females of comparable size, yet

surprisingly, they dismissed the possibility of biasing

of sex ratios through preferential male browsing.

Experimental manipulation of sex ratios in Atriplex

amnicola showed that maximum fruit fills were obtained when the population had 50 percent males

(Strawbridge and others 1997). However, optimum

seed productions were obtained within a relatively

wide range of shrub sex ratios (from 11 to 50 percent

males). These results are consistent with suggestions

made for A. canescens by McArthur and others (1978).

The breeding system of Atriplex is perhaps the

trait responsible for most of the complexities in

plant-herbivore interaction patterns that will be

described in subsequent sections. Most of the work

on breeding systems of Atriplex has been carried out

in A. canescens; however, surprisingly, almost no

work relating breeding systems to intraspecific variations in plant defense levels and browsing patterns

have been published for this species. The opposite

situation exists with A. vesicaria; relatively little has

been published about breeding systems and genetics

of the species compared to the volume of browsingrelated research results. Another unexpected fact is

that questions related to the induction of sex change

through browsing stress do not appear to have been

addressed in either A. canescens or A. vesicaria; but

see Maywald and others [in press].

Effects of Browsing on Shrub

Fitness ________________________

Survival and Reproduction

Fitness of Atriplex, understood as the “genetic contribution by an individual’s descendants to future

generations of a population” (Ricklefs 1990), may be

affected by browsing in a number of ways, ranging

from reproductive alterations to death of an individual. Trlica and others (1977) conducted a clipping

experiment to study the effects of rest following
USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998 9

defoliation on the recovery of A. canescens—among

other range species—on the shortgrass steppe. They

stated that six heavy defoliations at different phenological stages, from fall through late summer, “would

probably kill the plants” (p. 26). They also found that

a single defoliation near maturity (= producing flowers) was most harmful to plants relative to defoliations of equal intensity carried out at the phenological

stages of quiescence, early growth, or rapid growth.

Multiple defoliation treatments in fourwing saltbush

rendered smaller values of vigor (= subjective categories integrating measurements of live crown morphology with number and length of seedstalks), herbage

yield, and basal stem total nonstructural carbohydrate levels, relative to undefoliated shrubs (Buwai

and Trlica 1977). In this experiment, basal total

nonstructural carbohydrates levels were less affected

than herbage yield and plant vigor. No significant

differences among sexes were found in the response

variables these authors measured (Joe Trlica, personal communication). However, Tiedemann and others (1987) found seasonal differences in chlorophyll,

total nonstructural carbohydrates levels, and other

metabolites among ungrazed male, female, and labile

bushes. Differences were found only in the spring

when males had higher values than the other phenotypes. Buwai and Trlica (1977) suggested that fourwing

saltbush at their research site might not be affected by

either spring and fall, or spring and early summer

utilization. They also reported that three moderate

defoliations (removal of 60 percent of current year’s

growth) during rapid growth, seedset, and quiescence

stimulated twig growth. However, utilization at high

intensity (defoliation of 90 percent of current year’s

growth) and high frequency (four multiple defoliations) could kill the plants.

Pieper and Donart (1978) studied the effects of

defoliation by moderate browsing in a population of

Atriplex canescens in south-central New Mexico.

They found significant differences in basal and aerial

leader growth, and shrub mortality between browsing

frequency treatments. Over a 4 year period, shrubs

browsed for 3 years and protected during the last year

exhibited somewhat greater aerial leader growth

than those browsed continuously over the 4 years,

and even slightly greater aerial leader growth than

the protected plants. Basal leader production was

approximately four times larger in plants that received a year’s rest compared with shrubs that were

browsed throughout the period. Protected plants from

the exclosure produced no basal leaders, apparently

because basal buds were under apical dominance control. Mortality for a 7 year period of continuous browsing was nearly 25 percent, while less than 5 percent of

plants browsed for 3 years and protected for 4 years

were reported to have died. These authors concluded

that fourwing saltbush at this site required periodic

rest in order to survive and remain vigorous.

Price and others (1989) revisited and enlarged on

work carried out by Pieper and Donart (1978) and

stated that browsing with an adequate sequence of

rest can stimulate growth in fourwing saltbush. These

conclusions agree with results previously reported by

Buwai and Trlica (1977). Price and others (1989)

argued that grazing strategies, including a 60 day

deferment of shrubs during the early growing season,

would allow for adequate plant growth. They observed

that greatest damage to axillary buds of secondary

leaders (impairing adequate resprouting) occurred in

both continuously browsed shrubs and in shrubs

browsed after very lengthy rest periods, for different

reasons in each case. Browsing secondary leaders

when they were still tender and hae not become

slightly woody at their bases generally resulted in

damage to axillary buds. When more than 1 year of

rest was allowed, secondary leaders became very long,

woody, and brittle, and browsing caused the same

effect as with tender leaders. Rest periods of more than

1 year promoted progressively larger number of

flower stalks and less leader growth.

Eldridge and others (1990) conducted a study at a

number of sites of the Riverine Plains in Australia to

assess the effects of grazing by cattle and sheep on

Atriplex vesicaria (a dominant species within these

communities). The sites had been stocked at rates

recommended by the Soil Conservation Service of

New South Wales. They set up permanent transects

at intermediate distances from watering points and

followed individuals over a period of 7 years. They

found no differences in the way either cattle or sheep

browsing affected saltbush shrubs at the recommended

(moderate) stocking rates. Moderate grazing was reported only to affect shrub size, while overall fluctuations in density did not differ between grazed and

protected areas. Shrub population turnover was reported to be large (overall, about 50 percent per year)

in both grazed and ungrazed situations. In the past,

however, overgrazing of A. vesicaria-dominated

rangelands is known to have caused large mortalities

and replacement of this shrub by either grasses or

shorter lived chenopods over extensive areas (Stanley

1983). Fatchen (1978) revisited transects that had

been surveyed in 1932 in South Australia, and reported only four individuals of A. vesicaria compared

with the original 946 reported by researchers in 1932.

Fatchen (1978) was not able to establish the causes

for this decrease but suggested cattle and sheep grazing as a possible driving factor. Severe defoliations in

A. vesicaria led to shrub mortality in experiments on

areas of the northwestern Riverine Plain (Leigh and

Wilson 1970). In one experiment, paddocks stocked at

1, 0.5, and 0.25 sheep per acre suffered shrub mortalities of 100, 76, and 1 percent, respectively.
10 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998

An experiment where remaining leaves were

counted after each browsing event showed that bladder saltbush (Atriplex vesicaria) shrubs with less than

40 remnant leaves were unable to survive defoliation

under dry conditions. Apparently, under conditions of

severe defoliation, budded stems were removed by

sheep, thus preventing subsequent resprouting and

producing shrub death. According to Leigh and Wilson

(1970), A. nummularia (the dominant saltbush species over most of the southeastern Riverine Plain) is

more resistant to browsing than A. vesicaria, because

it can produce leaves from buds on main stems and is

capable of basal resprouting.

On mine reclamation lands grazed by cattle in

Wyoming, numbers of individuals in seeded Atriplex

canescens stands decreased dramatically throughout

a 5 year period (Schuman and others 1990). Booth

(1985) suggested that in such situations, A. canescens

might act as a pioneer species, and that its progressive decrease could be explained by its inability to

compete successfully with late seral species and by the

effect of browsing and basal decay. In another 5 year

experiment conducted on planted stands of A. nummularia and A. canescens in the northern Negev,

Israel, Benjamin and others (1995) studied the effects

of complete summer defoliation. Saltbush stands had

been planted at different densities ranging from 625 to

10,000 shrubs per ha and were browsed by sheep and

goats in some years, and by sheep alone in others.

Animals were taken off the pastures when all shrubs

had been completely defoliated. The authors measured shrub heights and widths and edible biomass

(twigs and leaves) before and after each defoliation

event. Neither A. nummularia nor A. canescens recovered their original crown sizes or biomass production

level. Leaf biomass regrowth tended to decrease progressively throughout the experiment period. Differences in biomass production between stands planted

at different densities, both on an individual and a

surface-unit basis, also decreased with time. The browsing treatment imposed on the shrubs caused large

mortality in A. canescens (at the end of the experiment

most of the shrubs in the high density plantation were

dead). Conversely, mortality was negligible in A. nummularia stands. A. nummularia actually out-yielded

both A. canescens and Cassia sturtii R.Br., a third

species included in the experiment. Malcolm and Pol

(1986) reported results from grazing trials on seeded

stands of A. amnicola (river saltbush), A. undulata

(wavy leaf saltbush), and A. padulosa (marsh saltbush), among others, on areas of bare saltland soils in

Western Australia. Browsing treatment imposed on

the seeded plots was severe—defined by the authors as

“...chewed back to sticks of about 5 millimeters thick”

(p. 60)—and occurred in autumn and early winter for

about 4 years. In one of the trials, marsh saltbush was

extirpated by the treatment, while survival in wavy

leaf saltbush and river saltbush was 54 and 94

percent. Recruitment of seedlings occurred in all

cases.

Hodgkinson and Baas Becking (1977) looked at the

effects of different defoliation treatments on root

growth in Atriplex vesicaria and A. nummularia. Both

interruption and resumption of root growth after

defoliation was slower in the shrubs compared to the

grass Danthonia caespitosa Gaudich (an abundant

perennial grass of Southern Australia). The authors

argued that reserve photosynthates in shrub stems,

on one hand, and a slower resumption of shoot growth

compared with the grass, on the other, could account

for shrub root growth response to browsing in this

experiment. According to these authors, the long period of root-growth depression in A. vesicaria could

explain its inability to cope with severe defoliation.

When both leaves and stems were removed, the situation became even more critical because reserves to

resume root-growth, contained in small twigs,

disappeared.

Examples from the previously mentioned literature

point to the fact that even though there appear to be

interspecific differences in response to browsing overall, important browse species of Atriplex are fairly

sensitive to high levels of defoliation. This condition

(browsing sensitivity) seems to be associated with

the removal of buds and subsequent resprouting

impairment. Of all species cited, A. nummularia and

A. padulosa appear to be the most resistant.

Browsing intensity and frequency might affect reproductive function by producing a decrease in numbers of seedstalks. Conversely, protection from browsing tends to have the opposite effect (Buwai and Trlica

1977; Price and others 1989). In A. canescens, shrub

size, also altered by browsing, can affect male and

female reproductive fitness differently. While smaller

males may be more efficient in dispersing pollen,

reduced size in females could lessen their ability to

intercept pollen, thus affecting their fecundity

(Freeman and others 1993).

Browsing and Drought Effects

Atriplex species exhibit a number of morphological

and physiological traits that enable them to cope with

drought. Some of these traits, reviewed by Newton and

Goodin (1989), involve: (1) regulation of leaf inclination (in A. hymenelytra); (2) production of leaf trichomes and accumulation of salt crystals on the leaf

surface to increase reflectance; (3) accumulation and

synthesis of inorganic and organic solutes to maintain

turgor; and (4) root association with endomycorrhizae

that allows absorption of soil moisture at very low

water potentials. Recently, molecular techniques
USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998 11

have been used both to study drought induction of

stress-protein synthesis and to identify specific genes

responsible for the synthesis of drought-induced mRNA

in A. canescens (Adair and others 1992). Such techniques, according to these authors, could help to understand the metabolism of drought tolerance mechanisms.

However, large scale shrub die-offs have occurred in

saltbush stands due to what may have been mixed

effects of browsing by large herbivores and drought.

Such interactions are not always clearly understood,

and have often been a source of controversy between

livestock operators and researchers (Stewart and

others 1940).

In a study reported in previous sections, Chambers

and Norton (1993) concluded that Atriplex confertifolia was sensitive to below-average precipitation years

and that browsing could aggravate stress in such

situations. Stewart and others (1940) also reported extensive shadscale die-offs due to the combined effects

of browsing and drought. However, timing and intensity of grazing might interact with drought, producing

opposite effects on plant population survival. Heavy

grazing or spring grazing of cold desert shrub communities in Utah were reported to have the most negative

effects on members of the plant community during a

period of drought. Conversely, winter grazing or light

grazing had beneficial effects on plants of the community during below average precipitation conditions

(Chambers and Norton 1993; Harper and others 1990;

Whisenant and Wagstaff 1991). In an analysis of

long-term data from the same site, Norton (1978)

found that 40 years of heavy winter grazing by sheep

did not produce any significant differences in density

and percent cover trend of A. confertifolia, Ceratoides

lanata, and Artemisia spinesens between grazed and

protected plots, supporting Chambers and Norton’s

(1993) observations.

Turner (1971) studied vegetation cover for a number of soil types at a salt desert site close to Grand

Junction, CO, for a period of 10 years (1953 to 1963).

He compared trends in grazed and protected watersheds and found that, even though drought and grazing resulted in overall deterioration of cover, shadscale

tended to increase its cover in the grazed watershed.

Turner (1971) attributed this to larger recruitment of

shadscale seedlings in the grazed pastures, which

could have balanced the loss of adult plants killed by

the drought. He also pointed to the fact that shadscale

(an armed saltbush) is not a shrub preferred by sheep

and cattle, and hence, grazing of competitors may

have released resources and facilitated establishment

of new plants.

In a study designed to determine the impact of

degree of defoliation, time of defoliation, and soil

moisture status on Atriplex vesicaria, Leigh and

Mulham (1971) found that completely defoliated

shrubs did not regenerate, irrespective of soil moisture status. They subjected shrubs to two treatments

of defoliation by sheep (severe and complete), and to

two conditions of soil water content (watered and

nonwatered) in February and October. While previous

research they cited had reported resprouting of

shrubs completely defoliated by drought deciduousness, they were not able to produce the same results in

watered shrubs completely defoliated by sheep. They

reported high mortalities in severely defoliated

shrubs that did not receive extra moisture by irrigation, especially when shrubs were left with less than

10 leaves and browsed in October. In moderately

grazed pastures of A. vesicaria, Eldridge and others

(1990) found greater rates of decrease in diameters

and heights of grazed shrubs compared with protected

shrubs during a drought period. Once conditions

were again favorable, after the drought, differences

disappeared. High mortality among old plants (over

30 years old) of A. vesicaria was reported to occur due

to drought (Crisp 1978). Anderson (1967) also pointed

to this fact, suggesting that larger “(and older?)” (p. 456)

shrubs might be the first ones to suffer the effects of

soil moisture deficit.

Work addressing the issue of drought-browsing interaction effects on saltbushes, relative to other aspects of saltbush biology, has seldom been reported in

the literature. Work reviewed in this section suggests

that factors such as intensity and timing of defoliation

together with the status of Atriplex within the browsed

community (whether it is dominant) may be crucial for

predicting the effect of drought-browsing interaction

on individuals.

Differential Browsing of Individuals Within

Populations

Work carried out in Atriplex vesicaria and A. canescens point to the fact that saltbush stands are not a

homogeneous browsing resource. There appears to be

a considerable amount of spatial and temporal variation associated with actual forage quality and availability of browsed Atriplex populations.

Female-biased herbivory in a population of bladder

saltbush in Australia was reported by Graetz (1978)

and Williams and others (1978). Osborn and others

(1932)were probably the first to report differential use

of Atriplex vesicaria shrubs in heavily browsed areas

around water points. Graetz (1978) and Williams

and others (1978) recorded sex ratios for several sites

and found that browsing by sheep promoted shifts

towards male-biased ratios. They suggested that preferential browsing of female individuals produced reduction in plant vigor and a consequent increase in susceptibility to death, by either drought or trampling,
12 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998

as the sex-biasing mechanism. A greater acceptability

of the female “green bladdery fruits” (p. 389), compared with male reproductive flowers, was offered as

a likely cause for sex-based selectivity of sheep. Vegetative vigor of male adult plants was found to be

greater than their female counterparts. This pattern

was particularly significant because density of seedlings was more strongly influenced by vigor of female

parents than by distance from pollen-producing

male neighbors. Maywald [personal communication]

is pursuing this topic and has reported that sheep

discriminate bladder saltbush on the basis of sex,

preferring to eat female plants and rejecting males.

Differential browsing in a heavily stocked population of fourwing saltbush in the Western United States

was also described by Otsyina (1983). He did not

report sex-related discrimination, yet stated that out

of a total of 700 shrubs (all exposed to high stocking

rates), one-third had been heavily browsed, one-third

had been moderately browsed, and less than one-third

had been lightly browsed. He suggested that variation

in concentration of saponins—a common secondary

compound in plants of the Chenopodiaceae—among

individuals was responsible for the browsing pattern

he observed. Differential grazing by rodents on a number of accessions of Atriplex canescens of different ploidy

levels grown in a common garden was reported by

Sanderson and others (1987). These authors found

sharp differences in the content of saponins between

accessions of A. canescens and postulated that this

may have influenced herbivore preference.

Sex-biased herbivory has been described for several

dioecious species, yet in the majority of cases plants

with male sex expression were reported to suffer

larger degrees of herbivory (Boecklen and others1990).

Examples of plant species where this is known to

occur include willows (Alliende 1989; Boecklen and

others 1990; Danell and others 1985), the dioecious

herb Rubus chamaemorus (Agren 1987), and the tree

Acer negundo (Jing and Coley 1990). A few authors

have reported cases of female-biased herbivory occurring, however, in species (Silene dioica and Rumex

acetosella) where male-biased herbivory also takes

place at some phenological stage (Lee 1981; Lovett

Doust and Lovett Doust 1985). Much of this research

has looked at the impact of invertebrate herbivores,

and cases reporting female-biased herbivory are based

on studies of smuts and rusts. Browsed Atriplex stands

are among the few cases in which sex-biased herbivory

has been addressed using large herbivores. However,

no clear pattern has yet emerged from such studies.

While female-biased herbivory has been found in sheep

browsing A. vesicaria (Maywald, personal communication) and in A. canescens browsed by heifers in

winter (Cibils and others, unpublished data), in a

study conducted on A. canescens during the growing

season, sheep preferred male over female individuals

(Maywald and others, in press). This same study

reported no preference in a winter grazing trial.

Further study of the causes and mechanisms of sexbiased herbivory in Atriplex would undoubtedly contribute to a deeper understanding of herbivory in

dioecious plants, an area that according to Boecklen

and others (1990) “...has been largely ignored in discussions of plant-animal interactions” (p. 586). These

examples suggest that browsing patterns controlled

by shrub gender-related differences in shrub palatability (perhaps as a consequence of defense chemicals) may be frequent in browsed Atriplex stands.

Defensive Chemistry of Atriplex ___

Defense Theory, Dioecious Plants, and

Atriplex

Plant defenses vary among species and range from

plant anatomical structures (thorns, for example) to

chemically active metabolites (Fox 1981; Zangerl and

Bazzaz 1992). Chemical plant defenses have been

classified into “quantitative” dose-dependent compounds that reduce diet digestibility in herbivores,

and “qualitative” compounds that are toxic to herbivores in relatively small doses (Feeney 1976; Rhoades

1979). Complexity of structures or metabolites and

their turnover rates determine the inherent costs of

synthesis and the maintenance of defense functions

(Zangerl and Bazzaz 1992). The idea of costs and

tradeoffs underlies most current theory on evolution of

plant defenses (Coley 1988; Coley and others 1985;

Feeney 1976; Herms and Mattson 1992; Rhoades

1979). A basic assumption of these models is that

plant fitness is closely related to cost:benefit relationships of allocating resources to defense under varying

conditions of resource availability, competition, and

selective pressure by herbivores (but see Bryant and

others 1985).

While plants living in different environments are

known to have strikingly similar tissue concentrations of carbon, water, and minerals, the ways in

which these resources are allocated to reproduction,

growth, and defense differ considerably. The fact that

these basic plant functions compete for limited resources has now been widely accepted (Bazzaz and

others 1987; Chapin and others 1987). Allocation patterns vary both spatially (between parts of a plant and

among individuals) and temporally (within a plant

over time) (Bazzaz and others 1987; Zangerl and

Bazzaz 1992).

Dioecious species offer interesting opportunities to

study intraspecific allocation patterns because each

individual has either male or female sexual expression. Harper (1977) stated that in certain dioecious
USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998 13

species, females allocated a larger amount of assimilates to reproduction and less to vegetative growth

than did males. Antos and Allen (1990, 1994) measured greater reproductive effort in female individuals

relative to males in the dioecious shrub Oemleria

cerastiformis. They reported that reproductive effort was twofold greater in terms of nitrogen and

fourfold greater in terms of biomass in females compared with males.

Tradeoffs derived from different reproductive efforts between sexes can induce slower growth rates

and smaller plant sizes in female individuals compared with males. Darwin (1877) demonstrated this

in an experiment with strawberry plants (but see

Gehring and Monson 1994). Intrinsic growth rate of a

plant species could determine the degree to which it

may allocate resources to defense (Coley and others

1985). In dioecious plants, this theory would predict

selection for greater levels of defense in female plants

because they have slower intrinsic growth rates relative to males. This could explain the fact that the

great majority of sex-biased herbivory examples have

been reported to be male-biased. An alternative hypothesis, which might explain female-biased herbivory,

reported for Atriplex is that reproductive investment

in females could constrain their ability to allocate

photosynthates to defense. Another possible explanation might be that a strong investment in defense of

reproductive structures could impair the ability of

female saltbushes to defend vegetative structures.

Certain accessions of Atriplex canescens have been

reported as containing relatively high levels of saponins, carbon-based plant defense compounds (Nord

and Van Atta 1960; Otsyina 1983; Sanderson and

others 1987). Nord and Van Atta (1960) examined

utricle bracts of fourwing saltbush and isolated saponins that they identified as a triterpenoid derived

from oleanolic acid. They reported very high contents

of saponins (10 percent of weight of original bract

chaff) and found this compound to have inhibitory

effects on germination in an experiment they conducted on seeds of fourwing saltbush and antelope

bitterbrush (Purshia tridentata [Pursh] DC). Recently,

Siddiqui and others (1994) isolated atriplexinol, a

triterpenoid sapogenin (the aglycone fraction of a

saponin, see next section), from A. stocksii Bois, a

saltbush that grows in marshes in subtropical and

temperate climates.

Davis (1981) reported relatively high levels of oxalates (in some cases potentially toxic) in 6 week old

greenhouse-grown plants of 14 species of Atriplex.

Oxalates occur in plants as either oxalic acid (a simple

dicarboxilic acid) or as calcium oxalate (an insoluble

compound with a low calcium:oxalate ratio). Animals

suffering acute poisoning by oxalic acid exhibit corrosion of digestive mucosas, nervous system alterations,

low blood coagulability, and renal insufficiency.

Animals consuming food with low levels of oxalates

may suffer chronic calcium deficiencies (Koplík and

others 1995). Anaerobic oxalate-degrading bacteria

were isolated fairly recently from the rumen, from

human feces, and from cecal contents of several animals. These bacteria use oxalates as a substrate. As

content of oxalates in the diet increase so do bacterial

populations and, therefore, toxic effects of these compounds are neutralized (Allison 1985). Allison argued,

however, that adjustments of bacterial population

size to level of oxalates require some time. Therefore,

ingestion of high levels of oxalates by animals that

have not undergone previous adaptation could cause

poisoning. Davis (1981) reported that concentrations

of oxalates varied among the 14 species of Atriplex he

studied, and they decreased over time in all species.

Seedlings of an Australian accession of A. leptocarpa

exhibited the highest oxalate content (12.6 percent),

while an accession of an unidentified species of Atriplex from Argentina yielded the lowest oxalate value

(4.2 percent). Levels of 8.7 percent (dry matter basis

inferred) of oxalate content were considered toxic

according to Dye (1956). By the time field-grown plants

were 6 months old, oxalate content had fallen below

toxic levels, and at 1 year of age the content had

dropped even lower. Oxalates have been reported in

variable quantities in other annual and perennial

chenopods of the United States (Halogeton glomerulatus and Sarcobatus vermiculatus) and Australia

(Maireana brevifolia, Chenopodium pumillo, Salsola

kali) (Jacob and others 1994; Morton and others

1959; Whitson 1994). Sporadic severe outbursts of

sheep poisoning with halogeton (Halogeton glomerulatus) have been attributed to the presence of toxic

levels of oxalates in this annual weedy chenopod

(Morton and others 1959).

Davis (1981) also measured tannin content in the

14 species of Atriplex he studied, and reported it to be

well below the levels required for animal rejection.

Tannins exhibit powerful astringent flavor and have

been defined as any polyphenolic compound with a

molecular weight greater than 500 (Liener 1980).

These substances have been classified as either hydrolyzable or condensed tannins, and are a relatively

common secondary compound in shrubs. Close to 79

percent of deciduous shrubs and 87 percent of evergreen shrubs contain them. Tannins can form complexes with either plant protein or animal digestive

enzymes, lowering protein availability to gut microbes

in ruminants, and producing growth-rate depression

in some monogastrics (Liener 1980; Rhoades and Cates

1976). Holecheck and others (1990) also reported low

content of tannins and soluble phenolics in fourwing

saltbush. In an analysis of 24 species from an AtriplexArtemisia community, Cates and McElroy (1987)
14 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998

reported that terpenes, cyanide, and alkaloids were

not detected in A. canescens specimens.

Other inorganic and organic compounds such as

selenium (Se) and the nonprotein nitrogenous compound glycinebetaine could also render certain Atriplex species either toxic or of low nutritional value to

browsers under certain environmental circumstances

(Booth 1985; Davis 1972; LeHouérou 1992). Selenium

toxicity occurs in most animal species when diets

contain 5 ppm of this mineral. In livestock, a disease

known as blind staggers that includes symptoms such

as loss of hair, hoof sloughing, lameness, blindness,

and paralysis followed by death is caused by an excess

of Se in the diet (Pond and others 1995). A number of

plants known as Se concentrators accumulate a considerable amount of this element when growing in

selenium rich soils. Such plants take Se from the soil

and concentrate it, mostly in the form of Se analog of

sulfur amino acids (Koplík and others 1995). All 15

native North American and introduced accessions of

Atriplex studied by Davis (1972) were found to concentrate Se when grown in selenium enriched soils. Three

accessions of A. canescens exhibited the highest Se

content.

Concentrations of glycinebetaine in water-stressed

Atriplex were reported to have increased as a means of

osmotic adjustment (Wynn Jones and Storey 1981).

They reported the presence of glycinebetaine (the

simplest of the N-methyl substituted amino acids,

commonly known as betaines) in 60 species of the

Chenopodiaceae, 14 belonging to the genus Atriplex.

Rumen microbes require an adaptation period and

energy supplementation to develop the ability to break

down glycinebetaine (Le Houérou 1992). However,

this compound is rapidly degraded by soil microbes

(Wynn Jones and Storey 1981), probably under aerobic conditions. Experiments conducted in vivo where

betaine-l-14C and betaine-methyl-14C were added to

the rumen of sheep showed that one of the products of

betaine metabolism, trimethylamine, was absorbed

from the rumen but was probably not used by the

animal. Addition of betaine-methyl-14C to the rumen

caused rapid increases of 14C labeled trimethylamine, followed by the excretion of 14C labeled trimethylamine oxide in the urine (Mitchell 1968).

Leaf surfaces exhibiting salt bladders are characteristic of some Atriplex species (A. hymenelytra, A.

confertifolia, A. lampa, and others). Under conditions

of drought, leaf bladders dry out allowing accumulations of salt crystals on the surface of the epidermis

(Kenagy 1972; Mares and others 1997; Mooney and

others 1977). While such salt accumulations are

thought to be primarily a water-saving adaptation of

desert halophytes (increasing leaf reflectance and

thus reducing leaf temperature and transpiration),

they can also act as a deterrent to herbivores. A few

desert rodents from North and South America (the

chisel-toothed kangaroo rat and the red vizcacha rat,

respectively) and from Northern Africa (the fat sand

rat) have evolved amazing adaptations to cope with

salt crystal accumulations on saltbush leaves. Such

adaptations include specialized lower incisors and

bristle bundles (groups of stiff hairs on either side of

the mouth), together with specialized kidneys that

allow these herbivores to shave the hypersaline tissue off leaf surfaces before consuming them and to

cope with diets containing large amounts of salts

(Degen 1988; Kenagy 1972; Mares and others 1997;

Schmidt-Nielsen 1964).

Among the secondary compounds found in Atriplex,

saponins are probably the most important. They are

the only plant defense metabolite in Atriplex, to our

knowledge, that has been reported to alter herbivory

patterns in both small and large browsers. While

apparently no published research has addressed the

issue of variation in content of saponins between

sexual phenotypes, among different plant parts, or

within individuals through time, the potential for

alteration of browsing patterns in Atriplex populations driven by variation in saponin contents definitely exists.

Saponins: Chemical Characteristics and

Mode of Action

Saponins are glycosides composed of a carbohydrate (L-arabinose, D-galactose, and D-glucose, for

example) and a noncarbohydrate or aglycone portion.

They are divided into two major groups on the basis of

the nature of the aglycone fraction (also known as

sapogenin or sapogenol) that can be either a triterpenoid or steroid derivative (Cheeke 1971; Price and

others 1987; Velisek 1995). Saponins are widely spread

among plants; nearly 100 plant families are known to

contain them. A number of plants used in both human

and animal feeding (some, such as spinach and sugar

beets are chenopod relatives of Atriplex) exhibit different amounts and types of saponins (table 1) (Price and

others 1987). Saponins present in legumes (such as

alfalfa and soybean) have been extensively studied

and belong to the triterpenoid type. Triterpenoids may

occur either as saponins or as sapogenins in the plants

that contain them. Steroid saponins, some of which

are available commercially (Sarsaponins), are derived

mainly from the yucca plant (Yucca spp.), and their

steroid moiety never occurs in the free sapogenin form

(Cheeke 1971; Valdez and others 1986). Identical

sapogenin moieties attached to different sugar chains

constitute a totally different saponin. The array and

numbers of individual saponins isolated are enormous. Mahato and Nandy (1991) listed over 270 triterpenoid saponins, isolated between 1978 and 1989
USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998 15

alone. Current chromatographic and spectroscopic

techniques, they argued, allowed greater efficiency

and accuracy in triterpenoid saponin isolation. Some

of the results of early research on the effects of saponins in foodstuffs on either humans or animals

were often contradictory, due in part to the inaccuracy

of the techniques available at that time (Price and

others 1987).

Plant materials containing saponins exhibit a bitter

taste, and tend to produce foam subsequent to agitation in aqueous solutions due to their activity in

lowering surface tension; hence, their name comes

from the Latin Sapo that means soap. Saponins have

also been described as able to hemolyze red blood cells,

and early assays to determine presence of saponins

were based on this property (Birk and Peri 1980).

Hemolytical properties of saponins in alfalfa were

probably one of the first aspects of their biological

activity to be studied. However, a large number of

biological effects (both negative and positive) have

been ascribed to the presence of these compounds.

Lysis of red blood cells is probably an example of the

most negative effects, while at the other end of the

spectrum are the ancient ginseng saponins from the

Chinese plant Panax (from the Greek “pan” = all, and

“axos” = cure) ginseng, with a great reputation as a

natural medicine with alleged anti-aging effects

(Price and others 1987; Velisek 1995).

Table 1—Some plant species containing saponinsa.

Contents measured as

Species percent of dry weightb

Plants used as foods and foodstuffs

Oats (Avena sativa) 0.1 to 0.13 (Rolled oats)

Sorghum (Sorghum sp.) .007 (seeds)

Millet (Pennnisteum sp.) .02 (seeds)

Spinach (Spinaceae oleracea L.) .7 to 4.7 (roots)

Tea (Thea sinensis L.) 13 (seeds)

Peanut (Arachis hypogaea) <0.001 to 1.6 (fruit)

Soya (Glycine max) 4.3 (beans)

Sugar beet (Beta vulgaris) 5.8 (leaves)

Asparagus (Asparagus officinalis L.) 1.5 (edible stalks)

Alfalfa (Medicago sativa) low saponin var. .14 to 5.6 (ground leaves and stalks)

Alfalfa (Medicago sativa) high saponin var. 1.71 (ground leaves and stalks)

Alfalfa (Medicago sativa) 8.0 to 8.7 (sprouts)

Alfalfa (Medicago sativa) .88 (roots)

Herbs and forbs

Yarrow (Achillea millefolium)

Tragacanth (Astragalus gummifer Labill.)

Wormseed (Chenopodium ambrosioides L.)

Pakistani ephedra (Ephedra gerardiana Wall. ex. Stapf)

Canaigre (Rumex hymenosepalus Torr.)

Dandelion (Taraxacum officinale Weber ex. wig)

a

Adapted from Price and others 1987, tables 2 , 5 , and 11, p. 33, 64, and 91. b

Where contents are not specified, presence but not levels of saponins were reported.

Several authors have written extensive reviews

on the biological effects of saponins (Birk and Peri

1980; Cheeke 1971; Mahato and Nandy 1991; Price

and others 1987). Cheeke (1971) summarized biological effects attributed to saponins as “1) erythrocyte

hemolysis; 2) effects on blood and liver cholesterol

levels; 3) effects on growth; 4) bloating of ruminants;

5) inhibition of smooth muscle activity; 6) enzyme

inhibition; 7) effects on nutrient absorption” (p. 622).

Birk and Peri (1980) also mentioned fungicidal and

bactericidal properties, together with insect-deterrent

effects and inhibitory effects on seed germination.

Ishaaya (1980) mentioned growth impairment in insects due to nonspecific association of saponins with

proteins that inhibited digestive enzymes and food

intake. Mahato and Nandy (1991) mentioned evidence

of molluscicidal activity and both antitumor and antileukemic activity of certain triterpenoid saponins.

Marston and Hostettmann (1991) also stressed the

value of molluscicidal action of saponins, stating that

their use could be valuable to control a number of snail

populations that act as intermediate hosts for human

intestinal parasites.

Most of the early work on effects of saponins in

foodstuffs were related to legume saponins fed to monogastrics. Many of the effects enumerated by Cheeke

(1971) were demonstrated either in experiments
16 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998

conducted in vitro or in feeding trials with monogastrics (mainly chicks and rats). According to

Cheeke (1971), little attention had been given to

ruminants where toxicity could only be demonstrated

when saponins were introduced directly into the blood

stream. He argued that biological activity was neutralized in the rumen where saponins were broken

down into their sugar and aglycone moieties. In ruminants, there appeared to be a considerable amount of

saponin breakdown by microbes in the gut, hence, the

low record on negative effects of orally introduced

saponins. Some in vitro experiments, where soybean

saponins were incubated both with washed microorganism-free tissue from ceca and colons, and with

cecal microflora alone, have shown that decomposition

of saponins into sapogenin and sugar moieties occurred only in the presence of cecal microbes. No

breakdown occurred in incubations with microbe-free

ceca (Applebaum and Birk 1979). Negative effects of

saponins in ruminants, according to the evidence

examined by Cheeke (1971), appeared to be mostly

restricted to the occurrence of bloat, a condition related to production of foam in the rumen and eructation impairment. Eventually, the accumulation of

gases in the rumen can put pressure on the diaphragm

muscle and cause heart failure or suffocation (Pond

and others 1995).

Saponins are also known to increase the permeability of membranes, a property that could alter absorption in the mammalian digestive tract, and that is

particularly dangerous for cold-blooded animals. Increased permeability of respiratory membranes in

fish and tadpoles causes rapid loss of respiratory

function and is, therefore, lethal (Price and others

1987). A considerable amount of research has focused

on the hypocholesterolemic effects of saponins.

Mechanisms that might account for this property are:

(1) these compounds affect the absorptive capacity of

intestinal mucosa by binding to membrane bound

sterols, triggering greater cell exfoliations, and with

them losses of cholesterol; and (2) saponins attach to

bile salts thus not allowing them to be reabsorbed in

the intestine, producing losses via feces of otherwise

reabsorbed cholesterol (Cheeke 1971; Gee and Johnson

1988).

Sarsaponins, sterol-derived saponins from the yucca

plant, have been reported to alter both protein metabolism by microorganisms in vitro, and ruminal

digestion and flow (Price and others 1987). However,

when these saponins were fed to dairy cows, no significant effect on rumen fermentation was found (Valdez

and others 1986). In this experiment the authors

reported that concentrations of ruminal ammonia,

blood urea, and volatile fatty acids were not different

between sarsaponin and control treatments. Another

trial using lambs with a different steroidal saponin

(smilagenin) reported improved growth rate of fattening lambs (Cheeke 1971). The structural similarity

of this saponin to diethylstilbestrol (a growth promotor) was suggested as the probable explanation for

the observed results.

The “bitter” or “astringent” taste ascribed to saponins

is thought to act as a herbivore deterrent. Some feeding experiments with poultry, rats, and swine showed

that these animals discriminated against diets with

high-saponin alfalfa, while rabbits were found to preferentially select high-saponin diets (Price and others

1987). Other sensory related effects of saponins were

reported in sheep consuming Tribulus terrestris, a

South African plant containing steroidal saponins

(Kellerman and others 1991). These authors were able

to induce hepatogenous photosensitization, a disease

locally known as geeldikkop, in an experiment in

which water-suspended steroidal saponins extracted

from T. terrestris were administered by stomach tube

to Merino lambs.

Secondary compounds in plants, acting as potential

antinutrients for herbivores, seldom occur in isolation. Interaction of saponins and tannins mixed in

diets was found to have positive effects on both rats

and ruminal microbia (Freeland and others 1985;

Makkar and others 1995). Freeland and others (1985)

conducted an experiment where mice were (1) allowed

to choose between food containing tannin or saponin, (2) given diets with tannins or saponins alone, or

(3) given diets with mixtures of predetermined amounts

of saponins and tannins. Mice that were allowed to

choose their own diets suffered none of the negative

effects (food-intake depression, loss of weight, or high

feces weight:food weight ratios) that were present

when they were fed diets with either tannins or saponins alone, or diets with both antinutrients in predetermined amounts. The authors postulated that

simultaneous consumption of tannins and saponins in

the right proportions may have produced interactions

that inhibited potential negative activity of either of

them alone. Makkar and others (1995) conducted in

vitro experiments with rumen liquor, adding different

types of tannins and Quillaja saponaria bark saponins. They reported that efficiency of microbial protein synthesis was higher with both saponins and

tannins added to the rumen liquor solution as compared to either tannic acid, quebracho tannins, or

saponins added alone.

The fact that Atriplex canescens contains triterpenoid saponins that have been shown to have deterrent,

hemolytic, and membrane altering effects in rats

may imply that patterns of ruminant herbivory could

be influenced by the presence of these chemicals.

Capability of saponins to affect rumen bacteria and

fungi should not be dismissed. However, because rumen microbes may break down saponins in the gut,
USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998 17

potential negative effects on metabolism may be neutralized; therefore, deterrent effects of saponin’s astringent taste may be the most important antiherbivore factor associated with these compounds.

Saponins in Other Chenopodiaceae

Recent studies have looked at saponin content of

Chenopodium quinoa (quinoa), an ancient Andean crop

known to be part of the diet of the Inca civilization.

Renewed interest in its nutritional attributes, mainly

due to the high protein content (14 to 18 percent) of

its seeds, has promoted research on quinoa saponins

regarding structure, content, and biological action

(Gee and others 1993). Quinoa saponins have been

divided, on the basis of their aglycon moiety, into those

containing (1) oleanolic acid, (2) hederagenin, and

(3) phytolaccageninc acid. Relatively little is known

about the mode of action of this last group (Gee and

others 1993; Price and others 1987). Differences in

types of sapogenins have been established between

lowland and highland varieties of quinoa in Peru

(Cuadrado and others 1995). Gee and others (1993)

performed in vitro and in vivo experiments with bitter,

washed bitter (debittered), and sweet quinoa grains.

They were able to show membranolytic activity of

isolated saponins in vitro, which increased small intestine membrane permeability. Rats in the in vivo

feeding studies showed marked aversion for the unwashed bitter flour and for grain diets containing a

proportion of unwashed bitter flour. Both intake and

conversion efficiency of the rats fed on bitter quinoa

flour was significantly lower to that of the other

groups. The authors postulated, on the basis of the

results of their in vitro experiments, that this could be

due to a significant decrease in intestinal function.

Other chenopods currently used in human and animal diets that have been reported to have saponins are

spinach (Spinacea olearacea) and sugar beets (Beta

vulgaris). Saponins from these chenopods are thought

to be triterpenoid saponins derived from oleanolic

acid, and in the case of the spinach plant, to have

hemolytic properties (Price and others 1987). Saponins

in these species, compared to other plant species

(table 1), are found in relatively high concentrations.

Nutritive Value of Atriplex as a

Forage for Ruminants ____________

The work described below dealing with the nutritional attributes of Atriplex spp. can be divided into

two main groups on the basis of the approaches followed. Authors from the first group, largely interested

in scanning plant resources for range reclamation,

have dealt mainly with the chemical composition of

plant edible material (generally leaves and fine stems)

and its variation between species, within a plant, and

throughout the growing season. A second group of

papers deals mainly with the effects of feeding saltbush diets to ruminants (mainly sheep and goats).

Different degrees of detail were pursued among authors of this second group, ranging from live-weight

monitoring in animals to measurements of digestibility of some key nutrients. Many of these trials

have compared performance of ruminants feeding on

Atriplex-based diets versus other conventional supplementation resources. Generally, feeding trials were

conducted with animals subjected to different degrees

of confinement, although at least two of the papers

reporting diet composition of free-ranging ruminants

are also included in this section. While there is a fair

amount of agreement among authors in the first

group, experiments conducted in the second group

have sometimes yielded inconsistent results.

Chemical Characteristics and Palatability

Many saltbushes exhibit a number of desirable forage attributes that have stimulated research on their

chemical and nutritional properties. High biomass

production, crude protein levels comparable to those

exhibited by alfalfa (table 2), evergreen foliage, resistance to drought, and high levels of salinity are some

of the outstanding traits reported in the literature.

However, low gross energy coupled with high mineral

content (mainly NaCl) and a relatively high proportion of nonprotein nitrogen call for special management techniques when using saltbushes as a forage

resource for ruminants (Glenn and others 1992).

Silva Colomer and Passera (1990) studied seasonal

variation in the chemical composition of six species

of Atriplex (A. lampa, A. nummularia, A. cinerea,

A. rhagodioides, A. bunburyana, and A. undulata)

from Tunisia, South Africa, and Spain. Most of the

chemical composition data from their experiment fell

within the ranges reported for North American saltbushes (table 2). They found levels of crude protein

and energy of a mixture of dried leaves and fine stems

to be remarkably constant across seasons and within

species. Crude protein content for most of the species

did not fall below 13 percent on any of their sampling

dates. The authors remarked on the high content of

phosphorous in the samples they analyzed. Monthly

variation of chemical components in leaves and

stems of A. polycarpa (Torr.) S. Wats., measured by

Chatterton and others (1971), showed a general decrease in protein, fats, and total digestible nutrients

during the summer months at a site in the San Joaquin

Valley, CA. Absolute values of each component fell

within the ranges reported (table 2). Winter protein

content was higher in both leaves and stems at this

winter-rainfall site, similar to that reported by Silva

Colomer and Passera (1990), for the measurements
18 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998

they conducted at sites with the same precipitation

regime. On the whole, Chatterton and others (1971)

reported that none of the nutrients they studied,

except for phosphorous at the end of summer, fell

below “nutritional requirements of a grazing animal”

(p. 37).

In an effort to establish the winter crude protein

content of Atriplex canescens, Welch and Monsen

(1981) measured nitrogen content of 43 accessions

grown in a common garden in Idaho. Accessions were

collected at a number of sites in Utah, Idaho, Wyoming,

Nevada, New Mexico, Arizona, and Montana. They

reported winter crude protein content ranging from

6.0 to 14.2 percent, with a large degree of variation

among accessions and between individuals within

accessions. Variation of coefficients of up to 33.9 percent were reported for crude protein content of individuals belonging to the same accession. The authors

pointed to the opportunities for artificial selection

presented by such great variability among individual

shrubs. Differences in crude protein, phosphorous,

and digestible organic matter among four accessions

of fourwing saltbush in western Texas were too small

to be considered biologically or nutritionally significant to herbivores (Petersen and others 1987).

Crude protein content (among other chemical constituents) of armed saltbush (Atriplex acanthocarpa

[Torr.] Wats) and fourwing saltbush were measured in

each of the four seasons, at a site in southern Texas,

where both of these shrubs grow together (Garza and

Fullbright 1988). Values of crude protein for leaves

and stems in armed saltbush were consistently higher

than in fourwing saltbush at all sampling dates. Crude

protein in leaves was remarkably high in armed saltbush (19 to 32 percent), and even though stem crude

Table 2—Comparative chemical composition of Atriplex spp. and alfalfaa.

Atriplex spp. Alfalfa (Medicago sativa)

aerial parts hay

Crude protein range 5.6 to 24.2 9.3 to 33.0

 (percent) mean 17.7 21.3

Fiber range 12.3 to 36.0 15.6 to 52.4

 (percent) mean 30.3 41.8

Cellulose range 12.5 to 29.0 17.0 to 38.0

 (percent) mean 20.8 27.5

Lignin range 9.5 to 16.0 5.0 to 18.0

 (percent) mean 17.5 14.0

Mineral content range 4.2 to 29.0 4.4 to 17.6

 (percent) mean 16.6 11.0

Gross Energy range 3.4 to 4.3 3.8 to 5.0

 (Mcal per kg) mean 3.9 4.4

a

From National Research Council (composition of cereal grains and forages) (1958).

protein values (9 to 20 percent) would be expected to

lower the overall value of edible biomass, this shrub

exhibited larger leaf:stem biomass ratios than

fourwing saltbush, enhancing interspecific crude protein differences. However, total standing crop per

plant was 5.6 times larger in fourwing saltbush, exhibiting average crude protein values for leaves and

stems that fell within the range of reported values

(table 2). The lowest crude protein content values (11.6

percent leaves, 4.6 percent stems) in fourwing saltbush at this site were reported for the month of

August, while the greatest values (23.7 percent leaves,

14.7 percent stems) were measured in February.

Khalil and others (1986) performed chemical analyses on leaves of six Atriplex species (A. nummularia,

A. canescens, A. vesicaria, A. rhagodioides F. Muell.,

A. lentiformis [Torr.] S. Wats, and A. undulata [moq.]

Dietr.) grown in Saudi Arabia. They found somewhat

higher crude protein content (16.7 to 25 percent) than

those reported for North American Atriplex spp.

(table 2). Sulfur amino acids were reported to be the

most deficient essential amino acids in all species,

while lysine content was close or above standard.

Digestible energy content reported ranged from 3.2 to

3.4 Mcal per kg. While rumen microbes are able to

synthesize all the amino acids classified as essential

for monogastrics, a general sulfur deficiency could

hinder microbial protein synthesis and could limit

animal function (Van Soest 1994).

Gross energy and mineral content of annual growth

in Atriplex canescens (measured as ash content and

combustion heat of oven-dried material) reported for

individuals from seven sites in Utah and Colorado was

within the expected range of values (table 2). Average

gross energy content (4.3 mcal per kg) was somewhat
USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998 19

higher than the values reported for greasewood

(Sarcobatus vermiculatus) (3.7 mcal per kg), yet lower

than in Artemisia tridentata (4.7 mcal per kg), Chrysothamnus nauseosus (4.8 mcal per kg), and Chrysothamnus linifolius (4.5 mcal per kg). Relatively high

content of essential oils and resins may account for

energy content of A. tridentata and C. nauseosus,

respectively (USDA 1937). Mineral content of fourwing saltbush (9.9 percent) was lower than in S. vermiculatus (20.2 percent), yet higher than in the other

shrubs included in the study (Van Epps and others

1982).

Young greenhouse-grown plants of 14 species of

Atriplex exhibited crude protein contents within the

ranges reported for North American Atriplex species

(table 2) in August and December measurements

(Davis 1981). Another greenhouse experiment with

young A. lampa designed to study the effects of water

stress on growth and nitrogen content was conducted

by Trione and Passera (1993). These authors reported

that while low water supply gradually reduced growth,

it did not affect nitrogen content of young saltbush

plants. They also found that A. lampa stored a large

amount of nitrogen (20 to 69 percent of total nitrogen)

in the free form (nonprotein nitrogen inferred), and

they related this to plant strategies of uptake and

utilization of nitrogen not affected by the water-stress

treatment.

Interplanting of fourwing saltbush into a seeded

stand of crested wheatgrass at Nephi, UT, was reported to promote increases in grass forage yield and

protein concentration, and to increase the total forage

biomass as well (Rumbaugh and others 1982). Protein

content of fourwing saltbush foliage in this experiment was twice the protein concentration of the

grass at all sampling dates.

Sims and Taylor (1973) obtained rather surprising results in an in vivo digestibility trial with rumen

fistulated steers on fourwing saltbush containing

5.6 to 11.5 percent crude protein (depending on

phenological stage) from the shortgrass steppe in

Colorado (table 3). They reported relatively low values of digestible crude protein in Atriplex. In fact,

during dormancy of the four species they studied

(Bouteloua gracilis, Agropyron smithii, A. canescens,

and Sphaeralcea coccinea), fourwing saltbush was the

species that exhibited lowest crude protein content.

Cook and others (1977), in a table on average nutritive

value of Colorado range plants, reported similar values of protein and digestible energy for both grasses

and the forb, but reported almost twice the winter

protein content for A. canescens.

Cattle diets, on sites with both sparse and abundant fourwing saltbush, on the shortgrass steppe

(Central Plains Experimental Range) were composed

of 23 percent (yearly average) fourwing saltbush

(Shoop and others 1985). Microhystological analysis

of feces showed that fourwing saltbush was the major

component of winter diets on the Central Plains Experimental Range (table 4). These authors stated

that 90 percent of the protein requirements and all the

metabolizable energy requirements of a dry pregnant

cow could be covered by a diet containing 33 percent

fourwing saltbush and 67 percent blue grama (on the

basis of the work by Cook and others 1977). Results

from cattle diet analysis on the shortgrass steppe,

reported by Shoop and others (1985), suggest that

when fourwing saltbush is abundant, cattle tend to

graze it preferentially. This strengthens apprehensions regarding the accuracy of Sims and Taylor’s (1973)

estimate of winter crude protein content for A. canescens

on the shortgrass steppe in Colorado. However, cattle

grazing a grass-fourwing saltbush mixture in Texas

during the month of January took considerably fewer

bites of fourwing saltbush compared to herbaceous

forage (Petersen and others 1994). These authors

Table 3—Comparative chemical composition and average digestibility of two grasses, a forb and a shrub from

the shortgrass steppea

.

Dry matter Crude Digestible Digestible

digestibilityb protein crude protein energy Ca P

- - - - - - - - - - - - - - Percent - - - - - - - - - - - - - - - Mcal per kg - - Percent - -

Bouteloua gracilis E 73 6.4 4.2 2.6 0.38 0.10

D 48 6.2 3.9 1.8 .27 .12

Agropyron smithii E 73 9.3 6.5 2.7 .20 .10

D 48 5.3 3.2 2.2 .22 .14

Atriplex canescens E 71 11.5 8.7 2.9 .89 .17

D 50 5.6 2.3 2.3 .82 .10

Sphaerelcea coccinea E 65 8.9 7.2 3.0 2.06 .15

D 71 9.0 7.3 3.2 2.53 .15

a

Adapted from Sims and Taylor (1973).

b

E = early growth (early spring); D = dormant (midwinter).
20 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998

attributed this to the fact that cattle were able to use

the herbaceous forage in a more efficient way. They

estimated that it would take cattle about 3 minutes to

consume as much shrub dry matter as they would

consume by feeding approximately 1 minute on herbaceous forage.

A study on diets of sheep grazing in Atriplex

vesicaria-dominated communities in Australia, however, revealed that animals discriminated against

dominant shrubs, preferring associated herbaceous

vegetation (Leigh and Mulham 1967). Palatability

studies of A. canescens carried out by Nemati (1977)

in Iran showed that A. canescens had intermediate

palatability compared with the native browse species

Artemisia herba alba and Kochia prostrata. The author

gave sheep free access to two levels (1.8 and 2.0 kg) of

availability of cuttings of each shrub and found that

the amounts of A. canescens consumed were smaller

than K. prostrata yet larger than A. herba alba.

Pearson and others (1990) conducted a browsing

experiment with interplanted individuals of A. vesicaria from six different populations that had been

historically submitted to either heavy or light grazing

by sheep. Their objective was to study the influence of

past grazing history on palatability of bladder saltbush to sheep. They suggested that plants with a long

history of heavy grazing were less palatable than

plants from the historically light-grazed populations.

However, they were not able to distinguish differences

in utilization of shrubs related solely to past history of

grazing. When flowering or fruiting status and salinity were added to their model, they found significant

differences in utilization (attributed to differential

palatability) between individuals with different histories of grazing. Pearson and others (1990) also reported greater heterogeneity in palatability among

plants with histories of heavy grazing than among

Table 4—Winter and summer diets of cattle on sites dominated by fourwing saltbush on the shortgrass steppea.

Winter Summer

Species Diet Species Diet

Site frequency composition frequency composition

- - - - - - - - - - - - - - - - - - - - - Percent - - - - - - - - - - - - - - - - - - - - -

Sandy plains and overflow sites (abundant saltbush)

Bouteloua gracilis 68.7 11 54.5 14

Agropyron smithii 21.3 19 24.8 15

Atriplex canescens 19.3 32 7.8 14

Sphaerelcea coccinea 21.8 2 64.8 5

Loamy plains site (sparse saltbush)

Bouteloua gracilis 66.0 7 62.9 18

Agropyron smithii 5.2 7 0.8 7

Atriplex canescens 0.1 3 0.1 1

Sphaerelcea coccinea 40.8 3 51.7 11

a

Adapted from Shoop and others (1985).

those with histories of light grazing. They hypothesized that grazing by sheep may have selected in

favor of less palatable phenotypes, thus increasing

heterogeneity. While the authors postulated interesting questions, their results do not appear to be

conclusive.

Overall, results from studies on chemical composition of edible biomass of Atriplex appear to coincide in

describing it as a high crude protein-low gross energy

forage. Palatability was generally described as intermediate to low, depending on species and season.

Performance of Ruminants Fed with

Atriplex Diets

Trials with sheep fed on diets based on Atriplex

vesicaria, A. nummularia, A. angulata, A. pyramidata,

and A. canescens have, in general, reported animals to

have maintained live weights (Atiq-ur-Rehman and

others 1990a,b; Kessler 1990; Wilson 1966a). Live

weight losses were reported for weanling Angora goat

kids that lost 40 g per head per day in a 34 day trial on

fourwing saltbush pastures (Ueckert and others1990a).

In this same experiment, however, animals grazing

saltbush with either forb-grass mixtures or with 32

percent crude protein supplementation were reported

to have gained weight. Live weight gains for yearling

Angora does grazing fourwing saltbush-grass mixtures were also reported for both wet and dry winters

(Ueckert and others 1992). Benjamin and others

(1992) reported no live weight gains in sheep consuming 1200 g per day (dry matter) of 18 percent crude

protein A. barclayana and up to 300 g of tapioca

supplement. However, these authors also reported

that live weight of sheep consuming a diet consisting

of 900 g per day (dry matter) of A. barclayana and

500 g per day (dry matter) of tapioca increased 3 kg
USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998 21

over a 30 day period (100 g per day). Trials conducted

in Pakistan, comparing performance of sheep grazing seeded stands of fourwing saltbush or native

mixed grassland-shrubland range, or native grazing

range with barley or alfalfa supplementation, showed

sheep gaining live weight in all treatments. However,

the lowest absolute live weight gain values were recorded for the saltbush diet (Atiq-ur-Rehman and

others 1990a). The author reported having found no

statistical differences between saltbush diets and either range grazing or range grazing plus barley grain

supplementation. This author argued strongly in favor of the use of Atriplex, not only for maintenance but

also to produce weight gains in sheep. Kessler (1990)

reported results from a trial in Saudi Arabia where

even though sheep herds feeding on A. nummularia

did not gain weight, they performed better than sheep

grazing unimproved rangeland which lost weight over

the trial period. Ueckert and others (1990b) found that

yearling ewes grazing a grass-fourwing saltbush

mixture during 60 days in winter gained 5.4 lb per

head. Conversely, yearling ewes wintered on a dormant warm season grass or on a grass-saltbush rotation during the same period lost weight.

Wilson (1966a,b) was able to assess the importance

of good quality drinking water (with low sodium chloride

content) as a factor regulating levels of consumption

of the Atriplex species he studied. Water with 0.9 to

1.2 percent NaCl depressed intake of A. nummularia

in sheep to half the levels otherwise obtained with lowsalt drinking water. The high content ( 3.2 to 8.2

percent) of sodium in the species of Atriplex used in

this feeding trial required sheep to ingest larger

amounts of drinking-water to be able to keep sodium

dilution proportions in the body constant. MacFarlane

and others (1967) reported a considerable amount of

variation between two sheep breeds (Border Leiceseter

and Merino) and among individuals of the same breed

in water turnover time and, consequently, total volume consumed, to cope with high electrolyte concentrations in Atriplex. They reported some sheep using

twice as much drinking water as others when browsing A. nummularia pastures.

Interplanting of Atriplex nummularia and A. vesicaria in natural grassland pastures had little effect on

total production and on seasonal fluctuations of wool

growth in another experiment conducted with Merino

wethers in Australia (Leigh and others 1970). Hobson

and others (1986) reported that a diet of A. nummularia

alone was not sufficient to provide the energy required

for pregnant Angora goat nannies. Supplementation

with a maize-based ration was required to avoid abortions and guarantee optimal fetal growth.

Several experiments cited by Glenn and others

(1992) were conducted with cattle, sheep, and goats to

test the ability of several Atriplex species to replace

traditional feeds, such as alfalfa hay. The results of

these studies suggested that some Atriplex species

could act as a substitute for alfalfa, provided they

were fed together with energy-rich foodstuff. An interesting feed lot experiment with crossbreed heifers

showed that A. undulata was as readily accepted as

alfalfa by animals that had not been preconditioned to

its use when it composed 20 percent of the ration.

Most feeding-trial studies have shown that ruminants fed with Atriplex diets tend to maintain body

weights. Claims regarding the possibility of body

weight gains in animals fed on saltbush diets do not

appear to be substantiated by most of the research

results reviewed. However, the value of Atriplex as a

forage resource may increase considerably when it is

fed to ruminants together with adequate energy

supplementation (but see table 5).

Metabolic Alterations in Ruminants

Consuming Atriplex

Weston and others (1969) conducted a 21-day digestibility trial with mature Merino wethers that were

kept in metabolism cages and fitted with ruminal and

abomasal cannulae. Several digestion parameters

(including flow of digesta and digestibility of organic

matter and protein) were measured for animals consuming leaves of Atriplex nummularia. The authors

had previously performed a similar experiment with

23 common pasture plants. They reported that values

Table 5—Nitrogen status of ruminants fed on Atriplex-based diets.

Species Diet N Intake Fecal N Urinary N N balance Reference

- - - - - - - - - - - - - g per day - - - - - - - - - - - - -

Sheep (A. nummularia) 16.3 3.5 14.9 –1.97 Hassan and others 1979

Goats (A. canescens) 8.0 2.0 7.0 –1.0 Ueckert and others 1990a

Goats (A. canescens) + concentrate 23.0 5.0 13.0 5.0 Ueckert and others 1990a

Sheep (A. barclayana) 16.6 4.5 9.1 3.0 Benjamin and others 1992

Sheep (A. barclayana) +100 g per day tapioca 17.8 5.3 9.4 3.1 Benjamin and others 1992

Sheep (A. barclayana) +200 g per day tapioca 18.3 5.7 9.7 2.9 Benjamin and others 1992

Sheep (A. barclayana) +300 g per day tapioca 18.9 5.9 7.8 5.2 Benjamin and others 1992
22 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998

of measured parameters for Atriplex fell within the

ranges observed in previous experiments, except for

two aspects of digestion. Saltbush “...deviated markedly from the others” (p. 520) in extent of digestion of

organic matter in the “stomach” (rumen?) and rate of

absorption of volatile fatty acids in the rumen. Because residence time for Atriplex in the rumen was

comparable to other forages, Weston and others (1969)

suggested that ruminal microbes could have suffered

metabolic alterations that prevented them from digesting fiber. A very low percentage of volatile fatty

acids was reported to be absorbed from the rumen, as

compared with other forages. A slight increase in

rumen pH was measured (+0.3 to 0.9), but according to

the authors, this could not account, by itself, for the

degree of absorption impairment. Finally, Weston and

others (1969) stated that the protein value of these

diets could be appreciably lower than what might have

been inferred from chemical analyses of the crude

protein. A large amount of the ingested crude protein

was degraded to ammonia in the rumen; the crude

protein in forms other than ammonia was stated to be

equivalent to 60 percent of the total content of forage

crude protein.

Questions related to the metabolism of nitrogen in

ruminants fed with the apparently protein-rich saltbushes have arisen repeatedly in a number of trials

with sheep and goats. A common element in trials

that have measured nitrogen inputs and outputs is a

surprisingly high level of urinary nitrogen, which sometimes causes a negative nitrogen balance in animals.

Several authors have related this phenomenon to the

low content of gross energy in saltbushes. However,

experiments in which animals that were fed on saltbush diets received energy supplementation did not

appear to confirm this hypothesis completely (table 5).

Hassan and others (1979) reported negative nitrogen balances in crossbred sheep consuming an average

of 801 g dry matter per day of hand-harvested leaves

and succulent stems of Atriplex nummularia. Six 43

kg animals were housed individually for 21 days in

metabolic cages. Urinary nitrogen losses measured by

the authors were more than 10 times higher (table 5)

than the predicted values of 1.4 g N per day for 43 kg

sheep, according to calculations made by Swanson

(1982). Fecal nitrogen losses were similar to those

predicted by NRC (1985) for 43 kg sheep (4 to 6.4 g N

per kg of dry matter consumed).

Ueckert and others (1990a) studied nitrogen balance of yearling Angora nannies fed ad libitum springgrowth leaves and twigs of fourwing saltbush, with

16 percent crude protein and 62 percent dry matter

digestibility, for a period of 20 days. Half the animals

received a diet of saltbush alone, while the other half

were fed a diet of saltbush leaves and supplement. The

supplement consisted of 300 g of 32 percent crude

protein concentrate for each animal per day. Goats

eating saltbush alone lost 88 percent of their daily

nitrogen intake in the urine, while goats fed on saltbush and concentrate lost only 57 percent of the

ingested nitrogen in the urine. An estimate of expected

daily urinary nitrogen loss for the goats in this experiment, under average conditions, would have been

approximately 1.27 g N per day (assuming a live

weight of 35 kg, and following Swanson’s (1982) estimate for sheep). Expected losses of fecal nitrogen, on

the other hand, can be estimated to range from 4 to

6.4 g of N per kg of dry matter consumed (NRC 1985).

Although animals were able to feed ad libitum, it

seems reasonable to assume consumption to have been

close to 1.1 kg of dry matter per day (close to 3 percent

of the animal’s live weight on a dry-matter basis).

While values of fecal nitrogen content were approximately within expected ranges (table 5), urinary nitrogen contents were consistently much higher than

what would otherwise have been expected.

Benjamin and others 1992 fed four 40 kg crossbred

male lambs a mixture of leaves and twigs of Atriplex

barclayana, either alone or mixed with different

amounts of tapioca (table 5). Each animal was randomly assigned one of the diets for a period of 9 days

(having been previously adjusted to the diet for 10

days); all animals were submitted to all diets. Even

though Benjamin and others (1992) did not find

negative nitrogen balances, the values for urinary

nitrogen were very high compared with expected value

(1.37 g N per day for 40 kg live weight, following

Swanson’s (1982) estimate for sheep). Again, fecal

nitrogen losses were within the expected range for

animals consuming 1,200 g of Atriplex and up to 300 g

of tapioca daily.

In both cases supplementation improved nitrogen

retention status but, overall, it was unable to bring

urinary nitrogen values down to normal ranges.

Ueckert and others (1990a) suggested, as possible

explanations for what they observed, that either plant

secondary compounds were interfering with nitrogen

retention, or plant crude protein was being hydrolyzed

in the rumen and rapidly absorbed as ammonia and

excreted in the urine. Benjamin and others (1992)

related the greater losses of urinary nitrogen, partly to

greater volumes of urine excreted in sheep consuming

Atriplex. They also stated that, as with other halophytes, Atriplex exhibited high mineral content and

high levels of nonprotein nitrogen, including quaternary ammonium compounds associated with salt tolerance mechanisms. Both of these characteristics,

they argued, would represent drawbacks in the

energy and nitrogen balances of ruminants consuming Atriplex diets.

Le Houérou (1992) argued that results showing

Atriplex as having little forage potential production
USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998 23

resulted from overly short feeding trials (2 to 5 weeks)

with unadapted animals. This author stated that in a

9 month trial conducted in Libya, sheep doubled

their initial intake of saltbush (A. nummularia and

A. canescens) over a period of 3 to 5 months (from 0.8-

1.2 to 1.5-2.5 kg digestible matter per head per day).

He reported that, with the levels of saltbush intake he

obtained in this trial, body weight of mature animals

could be maintained indefinitely, and that when saltbush was used as supplementation to grazing, live

weight gains could be expected.

Even if Le Houérou’s (1992) assertion about the

negative effect of short feeding trials on the assessment of forage attributes of Atriplex is accurate, the

fact that saltbush stands are often used to bridge

relatively short periods of forage scarcity still poses

interesting questions about its alleged qualities. If

livestock are fed on saltbush over a drought or winter

season (3 to 5 months average), they probably spend

most of the time adapting to Atriplex and are unable

to assimilate a large amount of its crude protein

content. Further research on gut microbe adaptation

times and processes is necessary.

Possible Management Implications

of Herbivore-Atriplex

Interactions ____________________

Research on aspects of the ecology of Atriplex reviewed in previous sections deals with three scenarios

that are not always explicitly addressed by the authors. The first one comprises situations in which

Atriplex is a dominant within the community; two

examples of this are the A. confertifolia- and A.

vesicaria-dominated communities. A second scenario

occurs with species from this genus that grow as local

populations within a community where Atriplex is

clearly neither a dominant species nor a strong competitor; A. canescens is a good example. Finally, there

are situations in which Atriplex has been seeded on

rangelands that have undergone some type of major

disturbance and that are subjected to fairly intense

management (irrigation, fertilization, rotation grazing); many species of Atriplex have been used in these

situations, but A. canescens and A. nummularia are

probably the most important. Generalizations and

comparisons across scenarios may not always be pertinent. Responses to browsing may differ in each case,

depending on the status of Atriplex within the community. A. confertifolia appears to be a clear example

of a saltbush species that under certain circumstances

is favored by grazing while the general trend is opposite. Even when it may seem contradictory, it is not

surprising that many of the saltbush species that are

considered a valuable browsing resource are the most

browsing-sensitive. They are, perhaps, the species

within the genus that have evolved less efficient defense mechanisms, and are thus unable to cope with

herbivory and competition successfully.

Variability, plasticity, and active population turnover are important characteristics of the genus that

have probably helped a number of Atriplex species

cope with herbivory. Half-lives of approximately 20

years (such as short generation times) can be expected

to favor perceptible heritable changes over relatively

short periods of time. History of browsing could potentially have strong effects on local populations by selecting for better defended, less palatable, and more

resistant genotypes. Clipping experiments and some

browsing research suggest that a number of saltbushes should be managed within very narrow boundaries of defoliation and rest to guarantee survival and

adequate reproduction. However, aspects of plant defense that may be able to control browsing patterns

under situations of reasonable use by browsers may

have been underestimated.

Spatial and temporal heterogeneity of the effective

browsing resource is probably a crucial issue in

browsed Atriplex populations. Such heterogeneity

stems from the interactions between breeding system,

defense ecology, age structure, soil patchiness, climate, and other factors. Differential defense of males

and females at different phenological stages can alter

seasonal availability of forage to browsers. The extent

to which a shrub is able to withstand defoliation and

still allocate carbon to defense could control the ability

of plants to influence browsing patterns through time.

The ability of some individuals to switch sexes and

potentially alter carbon allocation priorities could

change their defense capabilities, thus altering forage

availability to herbivores. Segregation of sexes across

the landscape (controlled by soil texture and moisture), coupled with differential levels of defensive

compounds in males and females may control distribution of browsers over small areas.

Results from feeding trials with Atriplex suggest

that chemical analyses of nutritional attributes of

saltbushes need to be interpreted with care, lest the

actual nutritional value in vivo be overestimated.

Further understanding of the interactions between

soil salinity and drought, with the relative amount of

nonprotein nitrogen compounds and minerals contained in edible tissues, may be an important key to

predicting the relative nutritive value of saltbushes.

Questions related to the metabolic pathways of nonprotein nitrogen compounds from Atriplex in ruminants, and their interaction with the digestible energy

content of the forage, may also be crucial to fairly

assess the amount of nitrogen from edible shrub

biomass that is effectively available for secondary

production. Ways in which secondary compounds
24 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998

from Atriplex might alter nitrogen metabolism in

ruminants also appear to require further research.

If sustainable browsing of saltbush stands is to be

attained, managers must take into account interactions occurring between herbivory and both interspecific and intraspecific competition in the plant

community. Unlike other shrub species, where recruitment events are rare and individuals are long-lived,

saltbushes are relatively short-lived and recruitment

events are fairly common. These processes, which

affect population turnover rates, appear to be far more

dynamic and sensitive to both biotic and abiotic factors

in saltbushes as compared to other shrubs. The success of management strategies for browsed saltbush

stands may depend, to a great extent, on the ability of

such strategies to balance rates of recruitment and

mortality of individuals.

Factors affecting recruitment appear to be more

closely related to competitive interactions (altered by

herbivores) than to the direct effects of browsing on

seed production or propagule survival. Competitive

interactions with other members of the plant community could limit recruitment success in many circumstances. Research reviewed in previous sections

indicates that in communities with A. confertifolia

increase in density of shadscale plants in grazed pastures, as compared to protected areas, could have been

a result of decreased competitive ability of the more

heavily browsed members of the community. Furthermore, different degrees of browsing on saltbushes,

affecting crown sizes and shrub density, could alter

the shrub interspace environment and indirectly affect conditions for recruitment by either facilitating or

hindering the establishment of potential competitors.

Further research is required to understand these

interactions.

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resistance to herbivores and pathogens. Ecology, evolution and

genetics. The University of Chicago Press: 363-391.
30 USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998

 Scientific name Common name

Acer negundo Boxelder

Achillea millefolium Yarrow

Agropyron smithii Western wheatgrass

Arachis hypogaea Peanut

Artemisia herba alba White sage

Artemisia spinesens Budsage

Artemisia tridentata Big sagebrush

Asparagus officinalis Asparagus

Astragalus gummifer Tragacanth

Atriplex barclayana

Atriplex acanthocarpa Armed saltbush

Atriplex amnicola River saltbush

Atriplex angulata

Atriplex bunburyana

Atriplex canescens Fourwing saltbush

Atriplex cinerea

Atriplex confertifolia Shadscale

Atriplex coriacea

Atriplex corrugata Mat saltbush

Atriplex cuneata Castle Valley clover saltbush

Atriplex falcata Falcate saltbush

Atriplex glauca

Atriplex halimus

Atriplex hymenelytra Desert holley saltbush

Atriplex lampa Zampa

Atriplex lentiformis Big saltbush

Atriplex leptocarpa

Atriplex leucolada

Atriplex litoralis Shore orache

Atriplex nummularia Oldman saltbush

Atriplex padulosa Marsh saltbush

Atriplex patula Spearscale

Atriplex polycarpa Allscale

Atriplex pyramidata

Atriplex repanda

Atriplex rhagodioides

Atriplex rosea Redscale

Atriplex semibaccata Fleshscale

Atriplex stocksii

Atriplex tridentata Saltsage

Atriplex undulata Wavy leaf saltbush

Atriplex vesicaria Bladder saltbush

Avena sativa Oats

Beta vulgaris Sugar beet

Bouteloua gracilis Blue grama

Cassia sturtii Senna

Ceratoides lanata Winterfat

Chenopodium ambrosioides Wormseed

Chenopodium pumillo

Appendix: Index of Scientific and Common Plant Names (some species have

no established common names) _____________________________________

(con.)
USDA Forest Service Gen. Tech. Rep. RMRS-GTR-14. 1998 31

Chenopodium quinoa Quinoa

Chrysothamnus viscidiflorus Douglas rabbitbrush

Chrysothamnus linifolius Spreading rabbitbrush

Chrysothamnus nauseosus Rubber rabbitbrush

Danthonia caespitosa Wallaby grass

Ephedra gerardiana Pakistani ephedra

Glycine max Soya

Grayia brandegei Spineless hopsage

Gutierrezia sarothrae Broom snakeweed

Halogeton glomerulatus Halogeton

Helianthus annuus Common sunflower

Kochia prostrata Forage kochia

Larrea tridentata Creosote bush

Maireana brevifolia Bluebush

Medicago sativa Alfalfa

Oemleria cerastiformis Indian plum

Panax ginseng Ginseng

Prosopis jubiflora Mesquite

Purshia tridentata Antelope bitterbrush

Quillaja saponaria Soap-bark tree

Rubus chamaemorus Cloudberry

Rumex acetosella Sour weed

Rumex hymenosepalus Canaigre

Salsola kali Russian thistle

Sarcobatus vermiculatus Greasewood

Silene dioica Red campion

Sphaerelcea coccinea Scarlet globemallow

Spineacea olearacea Spinach

Taraxacum officinale Dandelion

Thea sinensis Tea

Tribulus terrestris Puncture vine

Zea mays Corn

 Scientific name Common name

Appendix (Con.)
Cibils, Andrés F.; Swift, David M.; McArthur, E. Durant. 1998. Plant-herbivore interactions in

Atriplex : current state of knowledge. Gen. Tech. Rep. RMRS-GTR-14. Ogden, UT: U.S.

Department of Agriculture, Forest Service, Rocky Mountain Research Station. 31 p.

Atriplex is a widespread genus with species dispersed over almost all continents. Many

taxa within this genus perform outstandingly under a variety of stress conditions and are

often an important source of forage for herbivores. Such attributes have drawn the attention

of many researchers who have conducted extensive studies on Atriplex across a wide variety

of environments and management scenarios. This report reviews much of the literature

dealing with aspects of the biology of Atriplex from an animal-plant interaction perspective.

Keywords: saltbushes, shrub ecology, animal-plant interactions

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