• 

United States 

Department of 

Agriculture ., 

Forest Service 

Northeastern Forest 

Experiment Station 

General Technical 

Report NE-153 

FOREST INSECf GUILDS: 

P ~I*I'ERNS OF INTERACTION 

WITH HOST TREES 

Edited by: 

YURI N. BARANCHIKOV 

WILLIAM J. MATISON 

FRED P. HAIN 

THOMAS L. PAYNE 

Abakan, Siberia, U.S.S.R. 

August 13-17, 1989 
The use of trade, firm, or corporation names in this publication is for the 

information and convenience of the reader. Such use does not constitute an 

official endorsement or approval by the U.S. Department of Agriculture of 

any product or service to the exclusion of others that may be suitable. 

Statements of the contributors from outside the U.S. Department of 

Agriculture may not necessarily reflect the policy of the Department. 

COVER 

The insects on the cover are all European dendrophilous species: Nympha/is polychloros 

(Nymphalidae), Cimbex femorata (Cimbicidae), and Dasyneura rozkovi (Cecidomyiiydae). Mr. Victor 

Bakhtin (Krasnoyarsk, U.S.S.R.) was the artist. 
FOREST INSECf GUILDS: 

P A'l'I'ERNS OF INTERACfiON WITH HOST TREES 

Edited by: 

YURI N. BARANCHIKOV 

V.N. Sukachev Institute of Forest and Wood 

Siberian Branch of the U.S.S.R. Academy of Sciences 

Krasnoyarsk 660036 U.S.S.R. 

WILLIAM J. MATISON 

USDA Forest Service 

North Central Forest Experiment Station 

1407 S. Harrison Road, East Lansing, MI 48823 U.S.A 

and 

Department of Entomology 

Pesticide Research Center, Michigan State University 

East Lansing, MI 48824 U.S.A 

FRED P. HAIN 

Department of Entomology 

North Carolina State University 

Raleigh, NC 27695 U.S.A 

THOMAS L. PAYNE 

Department of Entomology 

Virginia Polytechnic Institute and State University 

Blacksburg, VA 24061 U.S.A 

Proceedings of a Joint IUFRO Working Party Symposium 

Abakan, Siberia, U.S.S.R. 

August 13-17, 1989 

General Technical Report NE-153 

U.S. Department of Agriculture, Forest Service 

Northeastern Forest Experiment Station 

100 Matsonford Rd., Suite 200 

Radnor, PA 19087 

1991 
This proceedings is the result of a symposium held in Abakan, Siberia, U.S.S.R., August 13-17, 

1989. It was organized under the guidelines of the International Union of Forestry Research 

Organizations. Five IUFRO Working Parties convened to achieve this exchange: S2.07-01 (Seed and 

Cone Insects), S2.07-05 (Bark Beetles), S2.07-06 (Population Dynamics), S2.07-08 (Gall Midges), and 

S2.05-06 (Mechanisms of Tree Resistance to Insects). 

The papers are arranged in three sections according to their subject matter: 1) general or 

theoretical papers, 2) highly mobile, external phytophages, and 3) poorly mobile, internal phytophages. 

The breakdown by external and internal feeding strategy was done to recognize that therein lies a 

fundamental dichotomy between the kinds of defenses employed by trees against these two broad 

classes of feeders. This is not to imply, however, that within each general class there are not still 

substantial guild-to-guild differences in plant defenses. There are. This was the subject of the 

symposium. 

This publication is the result of a joint effort between the Northeastern Forest Experiment 

Station and the North Central Forest Experiment Station, USDA Forest Service. It is symbolic of 

their strong support for IUFRO goals of facilitating worldwide research on the significant problems 

facing forest resource managers. 

ACKNOWLEDGEMENTS 

We gratefully acknowledge the support of the V.N. Sukachev Institute of Forest and Wood, 

Siberian Branch of the U.S.S.R. Academy of Science, and the U.S.S.R. State Committee for Forests. 

Without their unflagging commitment this symposium could not have materialized. In particular, 

Dr. A lsaev, Minister of State Forests, provided crucial sponsorship. 

We also thank Mrs. Svetlana Pusir for her very significant technical assistance. 

Over the course of more than one year, many people helped to bring this printed volume to 

fruition. To them, we are especially indebted because they donated substantial time from their busy 

schedules. We recognize them in alphabetical order: Bruce A Birr, Robert A Haack, Robert K. 

Lawrence, and William A Main. In addition, we thank Marilyn Brouwer and Robin Bolig for their 

exacting efforts in the technical editing and computer formatting of the entire volume. 

Finally, we thank the INRA Station de Zoologie Forestiere, Ardon-45160 Olivet, France, for 

providing work space and support while editorial chores (of WJM) were being executed. 

iii 
TABLE OF CONTENTS 

GENERAL THEORY ON PLANT/PHYTOPHAGE INTERACTIONS 

1. HOST-PLANT SPECIALIZATION IN NEEDLE-EATING INSECfS OF SWEDEN 

Christer BjOrkman and Stig Larsson . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 

2. SAWFLIES AND PONDEROSA PINE: HYPOTHETICAL RESPONSE SURFACES 

FOR PINE GENOTYPE, ONTOGENETIC STAGE, AND STRESS LEVEL 

Michael R. Wagner ................................................ 21 

3. DOES REPRODUCTION COMPROMISE DEFENSE IN WOODY PLANTS? 

Daniel A Herms and William J. Mattson .................................. 35 

4. PLANT REPRODUCTIVE ORGANS AND THE ORIGIN OF TERRESTRIAL INSECfS 

Georgy V. Stadnitsky ............................................... 47 

5. PREFERENCE OF DENDROPHAGOUS INSECfS FOR FOREST BORDERS 

Andrey V. Gurov . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50 

HIGHLY MOBILE, EXTERNAL PHYTOPHAGES 

6. WOODY PLANT GRAZING SYSTEMS: NORTH AMERICAN OUTBREAK 

FOLIVORES AND THEIR HOST PLANTS 

William J. Mattson, Daniel A Herms, John A Witter, and Douglas C. Allen . . . . . . . . . . 53 

7. VARIATION IN THE NUTRITIONAL PHYSIOLOGY OF TREE-FEEDING 

SWALLOWTAIL CATERPILLARS 

Matthew P. Ayres, Janice L. Bossart, and J. Mark Scriber ....................... 85 

8. DO DIFFERENCES IN INDUCIBLE RESISTANCE EXPLAIN THE POPULATION 

DYNAMICS OF BIRCH AND PINE DEFOLIATORS? 

Seppo Neuvonen and Pekka NiemelA . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103 

9. REPEATED DAMAGE OF LEAVES BY PHYLLOPHAGOUS INSECfS: IS IT 

INFLUENCED BY RAPID INDUCIBLE RESISTANCE? 

I.A Bogacheva . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113 

10. DOUGLAS-FIR NUTRIENTS AND TERPENES AS POTENTIAL FACTORS INFLUENCING 

WESTERN SPRUCE BUDWORM DEFOLIATION 

Karen M. Clancy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123 

11. PATTERNS OF NUTRIENT UTILIZATION IN THE NEEDLE-FEEDING GUILD 

Thomas Seeber Jensen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 134 

12. THE FOLIVORE GUILD ON LARCH (LARIX DECIDUA) IN THE ALPS 

W. Baltensweiler . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 145 

iv 
13. OUTBREAK OF ZEIRAPHERA RUFIMITRANA ON SILVER FIR HITHERTO 

UNKNOWNINSOUTHWESTGERMANY 

Hermann Bogenschutz . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165 

14. AN INSECf OUT OF CONTROL? THE POTENTIAL FOR SPREAD AND 

ESTABLISHMENT OF THE GYPSY MOTH IN NEW FOREST AREAS 

IN THE UNITED STATES 

Max W. McFadden and Michael E. McManus .............................. 

15. INTEGRATING HOST, NATURAL ENEMY, AND OTHER PROCESSES IN 

POPULATION MODELS OF THE PINE SAWFLY 

AA Sharov .................................................... 

16. BIOECOLOGY OF THE CONIFER SWIFT MOTH, KORSCHELTELLUS GRACILIS, 

A ROOT FEEDER ASSOCIATED WITH SPRUCE-FIR DECLINE 

172 

187 

William E. Wallner, David L. Wagner, Bruce L. Parker, and Donald R. Tobi . . . . . . . . . 199 

17. THE RECONSTRUCfiON OF LYMANTRIA DISPAR OUTBREAKS BY 

DENDROCHRONOLOGICAL METHODS IN THE SOUTH URALS 

Sergei Kucherov . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205 

18. IMPACf OF A SPRING DEFOLIATOR ON COMMON OAK 

Victor V. Rubtsov and Irina A Utkina . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 207 

19. TOLERANCE TO INSECf DEFOLIATION: BIOCENOTIC ASPECfS 

Andrey A Pleshanov, Victor I. Voronin, Elena S. Khlimankova, 

and Valentina I. Epova . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 211 

20. INSECf-PLANT INTERACI'IONS IN ANTHROPOGENICALLY 

TRANSFORMED ECOSYSTEMS 

Evgeny V. Koltunov, Victor I. Ponomarev, and Sergey I. Fedorenko 

21. DOES THE PLANT DEFEND ITSELF AGAINST LEAF-FEEDING INSECfS? 

213 

Paul M. Rafes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 215 

22. THE ROLE OF PHENOTYPE STRUCI'URE IN THE POPULATION DYNAMICS 

OF GYPSY MOTH IN THE LOWER DNIEPER REGION 

Nikolaj M. Derevyanko . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217 

POORLY MOBILE, INTERNAL PHYTOPHAGES 

23. NOVEL ASPECfS OF HOST TREE RESISTANCE TO LEAFMINERS 

Stanley H. Faeth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 219 

24. THE WITHIN-TREE DISTRIBUTION OF CATERPILLAR MINES 

Michail V. Kozlov and Yulia G. Koricheva ................................ 240 

25. ADELGID AND SCALE INSECI' GUILDS ON HEMLOCK AND PINE 

Mark S. McClure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256 

v 
26. ADELGID HOST INTERACTIONS WITH SPECIAL REFERENCE TO THE 

BALSAM WOOLLY ADELGID IN NORTH AMERICA 

F.P. Hain, R.G. Hollingsworth, F.H. Arthur, F. Sanchez, and R.K. Ross ............ 271 

27. SIGNIFICANCE OF PHYTOHORMONES IN SIBERIAN LARCH-BUD GALL 

MIDGE INTERACTION 

Rida M. Matrenina . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 288 

28. MANIPULATION OF HOST PLANT BIOMASS ALLOCATION AND RESOURCE 

REGULATION BY THE LARCH BUD GALL MIDGE 

Yuri N. Baranchikov ............................................... 291 

29. GALL MIDGES (DIPTERA: CECIDOMYIIDAE) IN FOREST ECOSYSTEMS 

Marcela Skuhrava . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293 

30. SEED GALLS OF SEMUDOBIA BETULAE (DIPTERA: CECIDOMYIIDAE) ON 

SPECIES OF BIRCH (BETULA SPP.) 

Vaclav Skuhravy .................................................. 298 

31. STRUCTURE, SPECIFICITY, AND EVOLUTION OF INSECT GUILDS RELATED 

TO CONES OF CONIFERS IN WESTERN EUROPE 

Alain Roques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3()() 

32. SEED PRODUCTION AND CONE-FEEDING INSEcrs OF PINUS PUMILA ON 

THE KAMTCHATKA PENINSULA: ASPEcrs OF COEXISTENCE 

PetrA Khomentovsky and L.S. Efremova ................................ 316 

33. IPS TYPOGRAPHUS AND OPHIOSTOMA POLONICUM VERSUS NORWAY SPRUCE: 

JOINT ATIACK AND HOST DEFENSE 

Erik Christiansen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 321 

34. RELATIONS BETWEEN WOOD-INHABffiNG INSEcrs AND FUNGI 

Nina P. Krivosheina . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 335 

35. ON THE ROLE OF THE TREE IN RELATION TO COLONIZATION BY 

IPS TYPOGRAPHUS L 

S. Bombosch . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 347 

36. INTERSPECIFIC OLFACTORY COMMUNICATION IN THE SOUTHERN PINE 

BARK BEETLE GUILD 

T.L Payne, M.T. Smith, M.C. Birch, and A Ascoli •......................... 352 

37. USING PHEROMONES IN THE MANAGEMENT OF BARK BEETLE OUTBREAKS 

Alf Bakke ...................................................... 371 

38. EFFECTS OF LARCH DEFENSES ON XYLOPHAGOUS INSECT GUILDS 

Galina I. Girs and Victor M. Yanovsky . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 378 

39. EFFECTS OF FIR SAWYER BEETLE ON SPATIAL STRUCTURE OF 

SIBERIAN FIR STANDS 

Vladimir L Gavrikov and Valentina P. Vetrova ............................. 385 

vi 
40. FIR SAWYER BEETLE-SffiERIAN FIR INTERACTION MODELING: 

RESISTANCE OF FIR STANDS TO INSECT OUTBREAKS 

Tamara M. Ovtchinnikova and Victor V. Kiselev . . . . . . . . . . . . . . . . . . . . . . . . . . . . 389 

41. CONIFER DEFENSES AND XYLOPHAGOUS INSECTS 

Alexandr S. Rozhkov and Galina I. Massel . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 391 

42. ATTRACTION OF SOME SCOLYTIDS AND ASSOCIATED BEETLES TO THE 

HOST VOLATILES a-PINENE AND ETHANOL 

Leif Martin Schroeder . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 393 

43. INFLUENCE OF PREDATORS AND PARISITOIDS ON BARK BEETLE 

PRODUCTIVITY 

Jan Weslien . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 396 

44. SEASONAL AND SPATIAL CHANGES IN THE STRUCTURE OF THE 

SUBCORTICAL INSECT COMMUNITY IN PINE FORESTS 

Ken Yoshikawa and Makoto Kasahara . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 397 

vii 
CONTRIBUTORS 

Numbers in parentheses indicate the page on which the authors' contributions begin. 

AlLEN, DOUGLAS C. (53), College of Forestry and Environmental Sciences, State University of 

New York, Syracuse, New York 13210 U.S.A 

ARTHUR, F. H. (271), USDA Stored Products Insects R & D Lab, Savannah, GA 31403 U.S.A 

ASCOLI, A (352), Department of Entomology, Virginia Polytechnic Institute and State University, 

Blacksburg, VA 24061 U.S.A 

AYRES, MATIHEW P. (85), Department of Entomology, Michigan State University, East Lansing, 

MI 48824 U.S.A 

BAKKE, AlF (371), Norwegian Forest Research Institute, Box 61, 1432 As-NLH, Norway 

BALTENSWEH.ER, W. (145), Institute of Plant Sciences, Division of Phytomedicine, 

ETH-Zentrum/CLS, CH 8092 Zurich, Switzerland 

BARANCHIKOV, YURI N. (291 ), V.N. Sukachev Institute of Forest and Wood, Siberian Branch of 

the U.S.S.R. Academy of Sciences, Krasnoyarsk 660036 U.S.S.R. 

BIRCH, M. C. (352), Department of Zoology, South Parks Road, Oxford, OX1 3PS United Kingdom 

BJORKMAN, CHRISTER (1), Department of Plant and Forest Protection, Swedish University of 

Agricultural Sciences, P.O. Box 7044, S-750 07 Uppsala, Sweden 

BOGACHEVA, l A (113), Institute of Plant and Animal Ecology, Ural Branch of the U.S.S.R. 

Academy of Sciences, 8 March Street, 202 Sverdlovsk 620144 U.S.S.R. 

BOGEN~ HERMANN (165), Forest Research Station, D-7800 Freiburg, Germany 

BOMBOSCH, S. (347), Institut fiir Forstzoologie der Universitat Gottingen, Biisgenweg 3, 

D-3400 Gottingen, Germany 

BOSSART, JANICE L. (85), Department of Entomology, Michigan State University, East Lansing, 

MI 48824 U.S.A 

CHRISTIANSEN, ERIK (321), Norwegian Forest Research Institute, N-1432 As-NLH, Norway 

CLANCY, KAREN M. (123), USDA Forest Service, Rocky Mountain Forest and Range Experiment 

Station, 700 S. Knoles Drive, Flagstaff, AZ 86001 U.S.A 

DEREVYANK.O, NIKOLAJ M. (217), 1.1. Shmalgauzen Institute of Zoology, Ukrainian Branch of the 

U.S.S.R. Academy of Sciences, Lenin Street, 15, Kiev, U.S.S.R. 

EFREMOVA, L. S. (316), Kamtchatka Forest Experiment Station, Far-Eastern Research Institute of 

Forestry, Kluchevskaya str., 24-2, Petropavlovsk-Kamtchatsky 683002 U.S.S.R. 

EPOV A, VALENTINA l (211 ), Siberian Institute of Plant Physiology and Biochemistry, Siberian 

Branch of the U.S.S.R. Academy of Sciences, Irkutsk 664033 U.S.S.R. 

viii 
FAE1H, STANLEY H. (219), Department of Zoology, Arizona State University, Tempe, AZ 85287 

U.S.A 

FEDORENK.O, SERGEY L (213), Institute of Forest, Ural Branch of the U.S.S.R. Academy of 

Sciences, Sverdlovsk U.S.S.R. 

GA VRIK.OV, VLADIMIR I.. (385), V.N. Sukachev Institute of Forest and Wood, Siberian Branch of 

the U.S.S.R. Academy of Sciences, Krasnoyarsk 660036 U.S.S.R. 

GIRS, GAUNA L (378), V.N. Sukachev Institute of Forest and Wood, Siberian Branch of the U.S.S.R. 

Academy of Sciences, Krasnoyarsk 660036 U.S.S.R. 

GUROV, ANDREY V. (50), V.N. Sukachev Institute of Forest and Wood, Siberian Branch of the 

U.S.S.R. Academy of Sciences, Krasnoyarsk 660036 U.S.S.R. 

HAIN, F. P. (271 ), Department of Entomology, North Carolina State University, Raleigh, NC 27695 

U.S.A 

HERMS, DANIEL A (35, 53), The Dow Gardens, 1018 W. Main St., Midland, MI 48640 U.S.A, and 

Department of Entomology, Pesticide Research Center, Michigan State University, East Lansing, 

MI 48824 U.S.A 

HOI.LINGSWOR1H, R. G. (271), Department of Entomology, North Carolina State University, 

Raleigh, NC 27695 U.S.A 

JENSEN, 1HOMAS SECHER (134), Zoological Laboratory, Institute of Zoology and Zoophysiology, 

University of Aarhus, DK-8000 Aarhus, Denmark 

KASAHARA, MAKOTO (397), Laboratory of Silviculture, Faculty of Agriculture, Kochi University, 

Monobe B200, Nankoku City, Kochi, Japan 783 

1{}-aJMANKOVA, ELENA S. (211), Siberian Institute of Plant Physiology and Biochemistry, Siberian 

Branch of the U.S.S.R. Academy of Sciences, Irkutsk 664033 U.S.S.R. 

KHOMENTOVSKY, PE1R A (316), Kamtchatka Department of the Environment, Far-Eastern Branch 

of the U.S.S.R. Academy of Sciences, Prospect Rybakov, 19-A, Petropavlovsk-Kamtchatky 683024 

U.S.S.R. 

KISELEV, VICI'OR V. (389), V.N. Sukachev Institute of Forest and Wood, Siberian Branch of the 

U.S.S.R. Academy of Sciences, Krasnoyarsk 660036 U.S.S.R. 

KOL1UNOV, EVGENY V. (213), Institute of Forest, Ural Branch of the U.S.S.R. Academy of 

Sciences, Sverdlovsk U.S.S.R. 

KORICHEV A, YUUA G. (240), All-Union Research Institute of Plant Protection, Pushkin 8, 

Leningrad 189620 U.S.S.R. 

KOZLOV, MICHAH.. V. (240), All-Union Research Institute of Plant Protection, Pushkin 8, Leningrad 

189620 U.S.S.R. 

KRIVOSHEINA, NINA P. (335), AN. Severtzov Institute of Evolutionary Animal Morphology and 

Ecology, U.S.S.R. Academy of Sciences, Moscow 117071 U.S.S.R. 

ix 
KUCHEROV, SERGEI (205), Institute of Plant and Animal Ecology, Ural Branch of the U.S.S.R. 

Academy of Sciences, Sverdlovsk 620008 U.S.S.R. 

LARSSON, S110 (1 ), Department of Plant and Forest Protection, Swedish University of Agricultural 

Sciences, P.O. Box 7044, S-750 07 Uppsala, Sweden 

MASSEL, GALINA L (391 ), Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch 

of the U.S.S.R. Academy of Sciences, Irkutsk 664033 U.S.S.R. 

MATRENINA, RIDA M. (288), V.N. Sukachev Institute of Forest and Wood, Siberian Branch of the 

U.S.S.R. Academy of Sciences, Krasnoyarsk 660036 U.S.S.R. 

MA1TSON, WilLIAM J. (35, 53), USDA Forest Service, North Central Forest Experiment Station, 

1407 S. Harrison Road, East Lansing, MI 48823 U.S.A, and Department of Entomology, 

Pesticide Research Center, Michigan State University, East Lansing, MI 48824 U.S.A 

McCLURE, MARK S. (256), Connecticut Agricultural Experiment Station, Valley Laboratory, 

P.O. Box 248, 153 Cook Hill Road, Windsor, cr 06095 U.S.A 

McFADDEN, MAX W. (172), USDA Forest Service, Northeastern Forest Experiment Station, 

100 Matsonford Road, Radnor, PA 19087 U.S.A 

McMANUS, MICHAEL E. (172), USDA Forest Service, Northeastern Forest Experiment Station, 

51 Mill Pond Road, Hamden, Cf 06514 U.S.A 

NEUVONEN, SEPPO (103) Department of Biology, University of Turku, SF-20500 Turku, Finland 

NIEMELA, PEKKA (103), The Finnish Forest Research Institute, Department of Forest Protection, 

P.O. Box 18, SF-01301 Vantaa, Finland 

OVfCHINNIKOV A, TAMARA M. (389), V.N. Sukachev Institute of Forest and Wood, Siberian 

Branch of the U.S.S.R. Academy of Sciences, Krasnoyarsk 660036 U.S.S.R. 

PARKER, BRUCE L. (199), University of Vermont, Department of Plant and Soil Science, Burlington, 

VT 05401 U.S.A 

PAYNE, T. L. (352), Department of Entomology, Virginia Polytechnic Institute and State University, 

Blacksburg, VA 24061 U.S.A 

PLESHANOV, ANDREY A (211), Siberian Institute of Plant Physiology and Biochemistry, Siberian 

Branch of the U.S.S.R. Academy of Sciences, Irkutsk 664033 U.S.S.R. 

PONOMAREV, VICfOR L (213), Institute of Forest, Ural Branch of the U.S.S.R. Academy of 

Sciences, Sverdlovsk U.S.S.R. 

RAFES, PAUL M. (215), Laboratory of Forestry, Uspenskoje Village, Odintzovo Region, Moscow 

Territory 143030 U.S.S.R. 

ROSS, R. K. (271), Department of Genetics, North Carolina State University, Raleigh, NC 27695 

U.S.A 

X 
ROQUES, ALAIN (300), Institut National de Ia Recherche Agronomique, INRA-CRF-Station de 

Zoologie Forestiere, Ardon 45160, Olivet, France 

ROZHKOV, ALEXANDR S. (391 ), Siberian Institute of Plant Physiology and Biochemistry, Siberian 

Branch of the U.S.S.R. Academy of Sciences, Irkutsk 664033 U.S.S.R. 

RUBTSOV, VICI'OR V. (207), Forest Science Laboratory, Moscow Branch of the U.S.S.R. Academy 

of Sciences, Uspenskoe, 143030 U.S.S.R. 

SANCHEZ, F. (271 ), Department of Chemistry, North Carolina State University, Raleigh, NC 27695 

U.S.A 

SCHROEDER, IEIF MARTIN (393), Swedish University of Agricultural Sciences, Division of Forest 

Entomology, S-750 07 Uppsala, Sweden 

SCRIBER, J. MARK (85), Department of Entomology, Michigan State University, East Lansing, 

MI 48824 U.S.A 

SHAROV, A A (187), Entomology Department, Moscow State University, Lenin Hills, Moscow 

119899 U.S.S.R. 

SKUHRA VA, MARCELA (293), Institute of Entomology, Czechoslovak Academy of Sciences, 

Branisovska 31, 370 05 Ceske Budejovice, Czechoslovakia 

SKUHRA VY, VACLA V (298), Institute of Entomology, Czechoslovak Academy of Sciences, 

370 05 Ceske Budejovice, Czechoslovakia 

SMI1H, M. T. (352), USDA-ARS, P.O. Box 87, Byron, GA 31008 U.S.A 

STADNITSKY, GEORGY V. ( 47), Technological Institute of Pulp and Paper Industry, Leningrad 

198092 U.S.S.R. 

TOBI, DONAlD R. (199), University of Vermont, Department of Plant and Soil Science, Burlington, 

Vf 05401 U.S.A 

UTKINA, IRINA A (207), Forest Science Laboratory, Moscow Branch of the U.S.S.R. Academy of 

Sciences, Uspenskoe, 143030 U.S.S.R. 

VEIROV A, VALENTINA P. (385), V.N. Sukachev Institute of Forest and Wood, Siberian Branch of 

the U.S.S.R. Academy of Sciences, Krasnoyarsk 660036 U.S.S.R. 

VORONIN, VICI'OR l (211), Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch 

of the U.S.S.R. Academy of Sciences, Irkutsk 664033 U.S.S.R. 

WAGNER, DAVID L. (199), University of Connecticut, Department of Ecology and Evolutionary 

Biology, Storrs, Cf 06268 U.S.A 

WAGNER, MICHAEL R. (21 ), School of Forestry, Box 4098, Northern Arizona University, Flagstaff, 

AZ 86011 U.S.A 

WAlLNER, WHLIAM E. (199), USDA Forest Service, Northeastern Forest Experiment Station, 

51 Mill Pond Road, Hamden, Cf 06514 U.S.A 

xi 
WESLIEN, JAN (396), Division of Forest Entomology, Swedish University of Agricultural Sciences, 

P.O. Box 7044, S-75007 Uppsala, Sweden 

WITIER, JOHN A (53), School of Natural Resources, University of Michigan, Ann Arbor, MI 48104 

U.S.A 

YANOVSKY, VICfOR M. (378), V.N. Sukachev Institute of Forest and Wood, Siberian Branch of the 

U.S.S.R. Academy of Sciences, Krasnoyarsk 660036 U.S.S.R. 

YOSHIKAWA, KEN (397), Laboratory of Silviculture, Faculty of Agriculture, Kochi University, 

Monobe B200, Nankoku City, Kochi, Japan 783 

xii 
HOST-PLANT SPECIALIZATION 

IN NEEDLE-EATING INSECTS OF SWEDEN 

CHRISTER BJORKMAN and STIG LARSSON 

Department of Plant and Forest Protection 

Swedish University of Agricultural Sciences 

P.O. Box 7044, S-750 07 Uppsala, Sweden 

INTRODUCTION 

It has been suggested that the enormous diversity of phytochemicals within the plant kingdom 

makes it impossible for one and the same insect species to exploit all plant species (Dethier 1954, 

Fraenkel 1959). Not surprisingly, the number and diversity of host plants utilized by different 

phytophagous insects are highly variable, and the specific selective pressures acting on them are still 

poorly understood (Bemays and Graham 1988, Strong 1988). Many hypotheses have been proposed to 

explain variations in host specificity among phytophagous insects. For example, there are those based 

on plant traits: plant defenses (Ehrlich and Raven 1964), plant apparency (Feeny 1976, Rhoades and 

Cates 1976), plant abundance (Root 1973), plant nutritional value (Mattson and Scriber 1987); those 

based on insect traits: degree of intimacy with the host plant (Mattson et al. 1988), neuronal capacity 

of the insect (Levins and MacArthur 1969) and finally those based on natural enemies' traits, e.g. the 

impact of generalist predators (Bernays and Graham 1988). 

In this paper we examine the predictions resulting from hypotheses based on plant characteristics 

and insect intimacy. We have used the data available in the literature on host ranges of Swedish 

needle-eating insects reported to feed on the three major conifer species native to Sweden: Scots pine 

(Pinus sylvestris), Norway spruce (Picea abies), and juniper (Juniperus communis). These species account 

for almost all of Sweden's coniferous flora. 

HYPOTHESES EXPLAINING HOST-PLANT SPECIALIZATION 

According to the plant apparency hypothesis, differences in tissue chemistry exist between longlived perennial plants that are easily discovered by insects (apparent) and annual ephemerals that are 

more difficult to discover (unapparent) (Feeny 1976, Rhoades and Cates 1976). Supposedly, apparent 

plants contain relatively large amounts of unspecific allelochemicals of low toxicity, high in molecular 

weight (e.g. tannins), whereas unapparent plants contain small amounts of specific, highly toxic 

allelochemicals with a low molecular weight (e.g. glucosinolates). These groups of allelochemicals have 

been called quantitative and qualitative, respectively, by Feeny (1976). Owing to these differences, 

polyphagous insects are associated mainly with apparent plants and monophagous insects mainly with 

unapparent plants. Being long-lived and large, conifers meet all the criteria of apparent plants. Hence 

one can predict that a majority of insects feeding on conifers will be polyphagous. However the 

apparency hypothesis further predicts that the types of allelochemicals will vary among tissues within a 

plant depending on tissue apparency. Analogous to between-species variation, apparent tissue (usually 

perennial), containing unspecific allelochemicals, and unapparent tissue (usually short-lived), containing 

more specific allelochemicals, should favor polyphagy and monophagy, respectively. 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

1 
According to the nutrition hypothesis, folivores that feed on nutrient-impoverished plants will 

have evolved special behavioral adaptations and digestive and metabolic systems that allow them to 

sequester nutrients from very dilute mediums (Mattson and Scriber 1987). Such adaptations should not 

in principle prevent them from also feeding on nutrient rich diets. Hence they have the capacity to be 

polyphagous if other factors are not limiting. Because the conifer species in this study tend to be 

adapted to nutrient poor sites, and characteristically have low concentrations of N in their needles 

(Tamm 1955), one might predict then that their phytophagous insects should tend to be polyphagous 

other things being equal. In fact, Holloway and Hebert (1979) reported that many species of 

macrolepidoptera feeding on conifers seem to be less specific in their choice of hosts than species 

feeding on Angiosperms. 

According to the Host Intimacy Hypothesis, host specialization by insects will be proportional to 

the amount of time and body surface area which is spent in direct contact with living tissues of the 

host plant (Mattson et al. 1988). The rationale is that high intimacy requires highly elaborate 

behavioral, physiological, and temporal adaptations with a host plant and that increasing intimacy will 

therefore impose concomitant specialization. Hence the intimacy hypothesis predicts that intimate 

species such as leaf miners should tend toward monophagy whereas nonintimate species such as free 

feeding Lepidoptera should tend toward polyphagy. 

METHOD AND DEFINITIONS 

Information about food plants utilized by each insect species was obtained from Escherich 

(1931), NordstrOm et al. (1941), Schwenke (1974, 1978, 1982), Winter (1983), and EhnstrOm (pers. 

comm.) but the appendices provide further details. Only insects reported to occur on juniper 

(Cupressaceae), Scots pine (Pinaceae), and Norway spruce (Pinaceae) have been included. Most of the 

literature data concern insect occurrence at the plant species level, but in some cases information at 

the genus level has also been included. 

Host-plant specialization is defined according to Cates (1980): insects are considered to be 

monophagous (Mono) if they utilize one or several plant species within a single genus, oligophagous 

(Olig) if they feed on two or more genera within one plant family or closely related families, or 

polyphagous (Poly) if they feed on plants from two or more families (i.e. at least one conifer and some 

angiosperm). Insect species feeding on one genus within the Pinaceae plus juniper, and insects feeding 

on two or more genera within the Pinaceae plus juniper, denoted MonoJ and OligJ respectively in the 

appendices, are included in the oligophagous group elsewhere. Chemistry and morphology are more 

similar between the two conifer families than between conifers and angiosperms (Thomas 1970), 

justifying our inclusion of insects denoted MonoJ and OligJ in the oligophagous group. 

With respect to numbers of insect species associated with various host plants, a good 

correspondence has been found between faunal lists derived from the literature and data based on 

extensive field sampling (Southwood et al. 1982, NiemeUi and Neuvonen 1983). Thus the coarse 

division of host range used in this study probably reflects actual conditions. 

Needles were classified as either young or old. The young included buds and current-year 

needles; the old group included needles > 1 year of age. 

2 
RESULTS 

Detailed information concerning the host plants utilized by individual insect species as well as 

their host ranges, needle-age utilization, and feeding modes are presented in Appendices A-D. 

No obvious trend in the degree of host-plant specialization is apparent when all insect species 

are considered (Table 1). However, the degree of specialization varies distinctly among feeding and 

taxonomic insect groups. Mining microlepidopterans are mainly monophagous (X2 = 13.38, p < 0.01, 

df = 2). The absolute monophagy among the sawflies is notable. Chewing micro- and 

macrolepidopterans are predominantly po~hagous, the microlepidopterans, however, not significantly 

so (X2 = 5.76, p > 0.05, df = 2, and X = 14.92, p < .001, df = 2, respectively). Beetles are 

mainly oligophagous. 

Table 1. Numbers of mono-, oligo-, and polyphagous species within different 

insect groups on Swedish conifers 

Insect group 

Microlepidoptera 

Chewing 

Mining 

Others 

Macrolepidoptera 

Hymenoptera 

Symphyta 

Coleoptera 

Larvae 

Adults 

All chewing spp. 

Total 

Monophagous 

2 

13 

7 

2 

28 

1 

2 

33 

55 

Oligophagous Polyphagous 

5 10 

6 0 

4 3 

16 21 

0 0 

3 0 

9 6 

33 37 

43 40 

Table 2. Degree of host-plant specialization among chewing insects as related 

to their needle-age (young vs. old) utilization on Swedish conifers 

(based on 14 Lepidoptera, one sawfly, and four Coleoptera species) 

Host range 

Monophagous 

Oligophagous 

Polyphagous 

Young needles 

0 

5 

5 

Old needles 

3 

1 

5 

3 
No association was found between the degree of host~plant specialization and needle-age 

utilization in chewing insect species (Table 2). 

The oligophagous group predominates on all three conifers, comprising ca. 45 percent of the 

total number of insect species on each of them (Fig. 1 ). The relative proportions of monophagous and 

polyphagous insects differ between the tree species. Juniper, with its high proportion of monophages 

and low proportion of ~lyphages, differs significantly from both spruce and pine (X2 = 9.59, 

p < 0.01, df = 2, and x2 = 6.15, p < 0.05, df = 2, respectively). Although spruce and pine do not 

differ significantly, the proportion of monophages is slightly higher on pine. 

DISCUSSION 

All conifer species studied must be regarded as highly apparent to insects searching for 

ovipositional sites and low in nutritive value. According to the apparency and nutrition hypotheses, 

insects feeding on these tree species should tend toward polyphagy. Our data show no such trend 

when all insect species are considered. On the contrary, less than one third (29 percent) are 

polyphagous (Table 1). However, such a crude comparison might be too superficial. A more realistic 

assessment might be achieved by comparing our results with the proportion of monophagous and 

polyphagous insect species in studies including less apparent and more nutritious plants. This is 

possible only with specific insect groups (see below). Juniper differs from both spruce and pine, 

furthermore, in having relatively more monophagous insect species (Fig. 1). However, differences 

between the three conifer species with respect to apparency and nutritional value appear to be small. 

Ideally, any attempt to explain host-plant specialization based on plant characteristics should at least 

take variation in feeding habits among insect feeding guilds into account. The selection pressure on 

the insect varies depending on the plant traits encountered during feeding. Although this fact was 

earlier pointed out by Feeny (1976), among others, it has often been ignored. For example, insects 

feeding internally, such as mining insects, might be able to avoid some plant allelochemicals that are 

compartmentalized in the plant (Feeny 1970, 1976, Cornell 1989). On the other hand, they might 

expose themselves more to rapidly inducible defenses, such as phytoalexins. Although the nutrition 

Spruce 

n=79 

Pine 

n=72 

Juniper 

n=17 

Figure 1. Relative proportions (%) of mono-1, oligo-0 , and polyphagous ... 

insect species on each of the three conifer species. Each bar equals 100%. 

n- number of insect species. 

4 
hypothesis was developed based on free-living Lepidoptera, other groups might be more sensitive to 

variation in nutrient concentrations. In the following, therefore, we have broken down our data into 

feeding guilds. 

Mining Microlepidopterans 

The fact that the main defense compounds in conifers (terpenes) are concentrated in clearly 

defined resin ducts (Bennett 1954) may have important consequences for mining insects. For example, 

one needle-mining micro lepidopteran (Exoteleia pinifoliella) utilizes only pine species whose needles 

have very few resin ducts, all of which are small. Thus this species appears to be avoiding the resinous 

defense of the host (Bennett 1954). Mining insects seem to be very specialized, irrespective of which 

food plants they utilize (Hering 1951, Claridge and Wilson 1982, Price 1983). This implies that the 

degree of host-plant specialization is determined by selective pressures other than those proposed by 

the apparency hypothesis. The intimate relationship between mining insects and their hosts can 

probably best explain the narrow host ranges of mining insects. For example, the need to adapt to the 

anatomy and phenology of the plant may determine the range of hosts that a miner can potentially 

exploit (Hering 1951). However, the high degree of specialization might actually be an artifact 

produced as a result of poor investigation of most mining insects (Connor et al. 1980, Powell 1980). 

Chewing Insects 

Generally, insects feeding externally on leaves and needles come into minimal contact with their 

host's chemieal defense. Among the chewing insects in this study, however, the monophagous species 

constitute as large a proportion as the polyphagous species when compared over all conifer species 

(32 percent and 36 percent, respectively). 

However, most of the monophagous species are sawflies (Table 1) and sawflies are 

predominantly monophagous, regardless of which type of plants they utilize (Hodkinson and Hughes 

1982, Shaw 1984). Neither the apparency nor the nutrition hypothesis predicts this monophagy. In 

contrast, the intimacy hypothesis does because conifer-feeding sawflies insert their eggs into the needles 

of their host, and needle morphology is an important factor in determining oviposition success (Ghent 

1959). The ability of females to find needles suitable for oviposition should therefore be strongly 

selected for. A behavioral adaptation of this kind could be a major reason for the prevalence of 

monophagy among needle-eating sawflies (Futuyma and Peterson 1985). Moreover, several conifer 

sawflies have evolved the ability to "detoxify" the defensive compounds produced by their hosts (Eisner 

et al. 1974, Larsson et al. 1986) and furthermore to use these substances in their own defense against 

natural enemies (Eisner et al. 1974, Morrow et al. 1976, Boeve and Pasteels 1985). This may be 

another reason why sawflies on conifers are so specialized. Thus the intimacy hypothesis is partially 

supported in the sawfly case. 

The predominance of polyphagy among chewing Lepidoptera accords with the predictions of all 

three hypotheses. In two other studies including insects feeding on less apparent, more nutritious 

plants, the proportion of polyphagous species was reported to be 54 percent and 32 percent (Holloway 

and Hebert 1979, Hodkinson and Hughes 1982, respectively), whereas in this study it was 52 percent. 

According to both the apparency and the nutrition hypotheses, however, one would expect relatively 

more polyphagous insect species on conifers than on plants of lower apparency and higher nutritional 

value. Thus one out of two comparisons with other studies supports these hypotheses. In principal, a 

species may behave as a generalist either because every individual is generalistic or because the species 

consists of specialized individuals or subpopulations (Van Valen and Grant 1970, Jaenike 1978, Singer 

1983). For herbivorous insects there are many examples of specialization among individuals and 

populations (Knerer and Atwood 1973, Fox and Morrow 1981, Singer 1983, Futuyma and Peterson 

1985, Ng 1988). Lasiocampa quercus provides one such example in this study (Appendix B). Until 

5 
more data have been accumulated on the nature of polyphagy in herbivorous insects, any general 

conclusion would seem premature. Nevertheless, it is possible that "true polyphagy" (i.e. generalistic 

individuals) is a rare phenomenon. For example, the cost of multiple detoxification systems might be 

too great for individual insects (Karowe 1989). 

Needle-Age and Degree of Specialization 

According to the apparency hypothesis, young tissue should be protected by qualitative defenses 

and thus there should be selection for specialization among insects feeding on such tissue. However, 

there is no correlation between needle-age utilized and degree of host-plant specialization in our data 

(Table 2). Results from studies of insects on deciduous trees support the apparency hypothesis (Cates 

1980, NiemelA 1983). This difference between conifers and deciduous trees with respect to degree of 

specialization and utilized tissue-age could be due to the fact that young needles develop more slowly 

than young deciduous leaves. Hence the absence of a correlation between needle-age and degree of 

specialization could be due to small differences in apparency between young and old needles. Still, 

there is evidence showing that young needles of jack pine (Pinus banksiana) and Scots pine contain a 

resin acid that repels sawflies normally feeding on old needles (Ikeda et al. 1977 and NiemelA et al. 

1982, respectively). It has yet to be determined whether other needle-eating insects are repelled by the 

same substances (Buratti et al. 1990). 

CONCLUSIONS 

The applicability of the examined hypotheses to Swedish needle-eating insects can be summarized 

in the following way. 1) Polyphagy predominates among chewing lepidopterans, thereby supporting all 

three hypotheses. However, the many examples of specialized individuals among polyphagous insects 

and the comparison of our results with those obtained in studies of macrolepidopterans on other plant 

species weaken this support. 2) The absolute monophagy among sawflies supports the intimacy 

hypothesis and may be attributable to the oviposition behavior of the female and the detoxification 

ability of the larvae. 3) Although data on the mining insects also supports the intimacy hypothesis, the 

impact of generalistic predators cannot be ruled out. 4) No correlation was found between utilized 

needle-age and host-plant specialization, possibly because small differences in apparency exist between 

young and old needles. 

The data presented here supply very little support for the apparency and nutrition hypotheses. 

In their defense, we readily acknowledge that they were never developed as explanations for host 

specialization by phytophagous insects. For this reason, then, they are too general as we have 

presented them. They treat herbivorous insects as a uniform group and do not distinguish between 

feeding guilds. It has become more and more apparent that insect feeding guilds must be treated 

separately if we are adequately to understand plant-insect interactions (Mattson et al. 1988, Cornell 

1989, Larsson 1989). The intimacy hypothesis, which distinguishes between insect feeding guilds, is the 

hypothesis given most support by the data obtained in our survey of the literature. 

SUMMARY 

The degree of host-plant specialization in needle-eating butterflies and moths (Lepidoptera), 

sawflies (Hymenoptera, Symphyta), and beetles (Coleoptera) occurring in Sweden has been examined 

based on data in the literature. 

No general trend was found when all insects were considered. However, a closer examination of 

certain feeding guilds revealed that 1) polyphagy is predominant among chewing Lepidoptera, 

6 
2) monophagy among the mining microlepidoptera and all sawfly species, and 3) oligophagy among 

beetles. 

No correlation was found between utilized needle-age and degree of host-plant specialization. 

A comparison of the relative numbers of monophagous, oligophagous, and polyphagous insect 

species on the three common conifers (i.e. Scots pine, Norway spruce, and juniper) in Sweden showed 

that the frequencies of oligophagy are similar for each of the conifer species. However, the proportion 

of monophagous species was found to be significantly greater in juniper than in pine and spruce. 

These results are discussed with reference to hypotheses concerning patterns of host specificity in 

herbivorous insects based on plant characteristics. 

ACKNOWLEDGMENTS 

We would like to thank Bengt EhnstrOm and Karl-Johan Hedqvist for providing information on 

the biology of the insects. We also thank Hubertus H. Eidmann, J. Mark Scriber, Donald Strong, and 

David Tilles for helpful comments on the manus(.Tipt. 

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buoliana (Schiff.), in southern Ontario. II. Egg, larva and pupa. Can. Entomol. 95: 844-873. 

POWELL, J.A. 1980. Evolution of larval food preferences in microlepidoptera. Annu. Rev. Entomol. 

25: 133-159. 

PRICE, P.W. 1983. Hypothesis on organization and evolution in herbivorous insect communities, 

p. 559-596. In Denno, R.F. and McClure, M.S., eds. Variable Plants and Herbivores in Natural 

and Managed Systems. Academic Press, New York. 

RHOADES, D.F. and CATES, R.G. 1976. Toward a general theory of plant antiherbivore chemistry. 

Recent Adv. Phytochem. 10: 168-213. 

ROOT, R.B. 1973. Organization of a plant-arthropod association in simple and diverse habitats: the 

fauna of collards (Brassica oleracea). Ecol. Monogr. 43: 94-124. 

SCHNAIDER, Z 1976. Atlas uszkodzen drzew i krzewow. Panstwowe Wydawnictwo Naukowe, 

Warzawa. 

SCHWENKE, W. 1953. Beitrtige zur Bionomie der Kiefernspanner Bupalus piniarius L. und Semiothisa 

liturata Cl. auf bionOtischer Grundlage. Beitr. Entomol. 3: 168-206. 

SCHWENKE, W. 1974. Die Forstschttdlinge Europas. Bd. 2. KAfer. Paul Parey, Hamburg-Berlin. 

SCHWENKE, W. 1978. Die Forstschttdlinge Europas. Bd. 3. Schmetterlinge. Paul Parey, 

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Hamburg-Berlin. 

10 
SCHWERDTFEGER, F. 1970. Waldkrankheiten. Aufl. 3. Paul Parey, Hamburg-Berlin. 

SHAW, M.R. 1984. Insects associated with birch. Proc. R. Soc. Edinb. Sect. B/Biol. Sci. 85: 169-181. 

SINGER, M.C. 1983. Determinants of multiple host use by a phytophagous insect population. 

Evolution 37: 389-403. 

SOUTHWOOD, T.R.E., MORAN, V.C., and KENNEDY, C.E.J. 1982. The assessment of arboreal 

insect fauna: comparison of knockdown sampling and faunal lists. Ecol. Entomol. 7: 331-340. 

SPULER, A 1913. Die sogenannten Kleinschmetterlinge Europas. E. Schweizerbartsche 

Verlagsbuchhandlung, Stuttgart. 

STRONG, D.R., ed. 1988. Insect host range. Ecology 69: 885-915. 

TAMM, C.O. 1955. Studies on forest nutrition. I. Seasonal variation in the nutrient contents of conifer 

needles. Medd. Statens Skogsforskningsinst. 45(5). 34 p. 

THOMAS, B.R. 1970. Modern and fossil plant resins, p. 59-79. In Harbome, J.B., ed. Phytochemical 

Phylogeny. Academic Press, London. 

TRAGARDH, I. 1915. Bidrag till ldinnedomen om tallens och granens fiender bland smafjfirilama. 

Medd. Statens SkogsforsOksanst. 12: 71-132. 

TRAGARDH, I. 1939. Sveriges skogsinsekter. Gebers forlag, Stockholm. 

VAN V ALEN, L and GRANT, P.R. 1970. Variation and niche width reexamined. Am. Nat. 

104: 589-590. 

WINTER, T.G. 1983. A catalogue of phytophagous insects and mites on trees in Great Britain. 

For. Comm. Edinb. 

11 
APPENDIX A 

Host-plant utilization, host range, utilized tissue-age, and feeding mode of 

microlepidoptera feeding on Swedish conifers. Information on the occurrence 

of individual species in Sweden was taken from Gustafsson (1979); reference 

not provided. 

Family Host Host Tissue Feeding 

Species plants1 range2 age3 mode4 References 

Yponomeutidae 

Argyresthia abdominalis Zell. Jun Mono ? M 1,2 

A. arceuthina Zell. Jun Mono ? BM 1,2 

A. aurulentella Stt. Jun Mono ? M 1,2 

A. dilectella Zell. Jun Mono ? M 1,2 

A. £undella F.v. Rosl. Pic, (Abi) Olig Y+O M 2,4,5 

A. glabratella Zell. Pic Mono y M 1,4 

Blastotere bergiella Ratz. Pic Mono y M 4 

Cedestis gysseleniella Zell. Pin, (Abi) Olig 0 M 1,4,6 

c. sub£asciella Steph. Pin Mono 0 M 1,4,6,7 

Ocnerostoma £riesei Svensson Pin Mono ? M 1,7 

0. piniariella Zell. PIN,Jun OligJ ? M 1,4,7,10 

Gelechiidae 

Dichomeris juniperella L. Jun Mono ? c 1 

D. marginella F. Jun Mono 0? c 1,3 

Exoteleia dodocella L. Pin Mono Y(O) M 1,4,10,11 

Momphidae 

Batrachedra pinicolella Zell. Pic,Pin Olig ? M 1,3 

Tortricidae 

Acleris abietana Hb. PIN Olig Y+O c 1,4,8,12 

A. hyemana Haw. PIN,D Poly ? c 1,8 

Aphelia paleana Hb. Pic,H Poly ? ? 1,8 

A. v iburnana Den. & Schiff. PIN,D,H Poly y c 1,4,8 

Archips oporana L. PIN ,Jun Olig Y+O c 1,4,6,12 

A. podana Scop. PIN,D Poly Y+O c 1,4,12 

A. rosana L. Pic,D,H Poly ? c 1,4,5,10 

Blastesthia posticana Zett. Pin Mono y M 1,4,10 

B. turionella L. Pin,H Poly y M 1,4 

Clepsis senecionana Hb. PIN,H Poly ? M 1 

Cnephasia incertana Treit. PIN,H Poly ? M-+C? 4,8 

Epinotia caprana F. Pin,D Poly ? c 1,8 

E. £raternana Haw. PIN Olig 0 M 1,4,8 

E. nanana Treit. Pic Mono 0 M 1,4,10 

E. nigricana H.-S. Abi, (Pic) Olig y BM 1,4 

E. pygmaeana Hb. Pic, (Abi) Olig Y(O) M-+C 1,4 

E. rubiginosana H.-S. Pin Mono ? M-+C 1,8,10 

12 
APPENDIX A continued 

Family 

Species 

Host Host Tissue Feeding 

E. subsequana Haw. 

E. tedella Cl. 

Olethreutus lacunana 

Den. & Schiff. 

Pandemis cinnamomeana Treit. 

Philedone gerningana 

Den. & Schiff. 

Philedomides lunana Thnbg. 

Ptycholoma lecheana L. 

Rhyacionia buoliana 

Den. & Schiff. 

R. duplana Hb. 

R. pinicolana Doubl. 

R. pinivorana Zell. 

Spilonota laricana Hein. 

Zeiraphera diniana Guen. 

Z. ratzeburgiana Ratz. 

Cochylidae 

Aethes rutilana Hb. 

Pyralidae 

Dioryctria abietella 

Den. & Schiff. 

D. mutatella Fuchs 

D. schuetzella Fuchs 

plants1 

Abi, Pic 

Pic 

Pic,D,H 

PIN,D,H 

Pic,D,H 

PIN,D,H 

Pic,D 

Pin 

Pin 

Pin 

Pin 

Lar, (Pic) 

Pic,Pin 

PIN 

Jun 

PIN 

Pin 

Pic,Abi 

range2 

Olig 

Mono 

Poly 

Poly 

Poly 

Poly 

Poly 

Mono 

Mono 

Mono 

Mono 

Olig 

01* 

Olig 

Mono 

Olig 

Mono 

Olig 

age3 

y 

(Y)O 

? 

Y+O 

? 

? 

? 

Y(O) 

y 

y 

y 

y 

y 

y 

? 

y 

y 

y 

mode4 References 

M 

M 

c 

c 

c 

c 

c 

M(BM) 

BM 

BM 

BM 

C-+M 

C(BM) 

C(BM) 

c 

BM 

BM 

c 

1,4 

1,4,13 

1,4,8 

1,3,4,12 

1,3,8 

1,8 

1,4 

1,4,14 

1,4 

1,4 

1,4 

1,4 

1,4,10 

1,4 

1,9 

4 

1,4 

1,4 

* The Picea-Pinus-race that might be a species (two other races exhibit other 

host plant preferences) 

1 Abi =Abies, Lar = Larix, Pic = Picea, Pin= Pinus, and Jun = Juniper; PIN = 

several spp. within Pinaceae; D indicates that the insect species utilizes one 

or several deciduous trees or bushes; H indicates that it utilizes one or 

several herbaceous plant species. 

2 Mono - monophagous, Olig = oligophagous, OligJ - feeding on some member of 

Pinaceae and Juniper, and Poly= polyphagous. 

3 Y = young tissue (buds and current-year needles) and 0 

(1-year-old or older needles). 

old tissue 

4 C =chewing, M =mining in needles, BM mining in buds (and/or shoots). 

Arrows under Tissue-age and Feeding mode indicate that the insect shifts from 

~y when it becomes older. 

13 
REFERENCES: 1) Winter (1983), 2) Escherich (1931), 3) Spu1er (1913), 

4) Schwenke (1978), 5) Schnaider (1976), 6) TrAgardh (1915), 7) Hannemann 

(1977), 8) Hannemann (1961), 9) Hannemann (1964), 10) Browne (1968), 11) Martin 

(1959), 12) Patocka (1960), 13) FUhrer (1967), and 14) Pointing (1963). 

14 
APPENDIX B 

Host-plant utilization, host range, utilized tissue-age, and feeding mode of 

macrolepidoptera feeding on Swedish conifers. Information on the occurrence of 

individual species in Sweden was taken from Elmqvist et al. (1977); reference 

not provided. 

Family Host Host Tissue Feeding 

Species plants1 range2 age3 mode4 References 

Geometridae 

Biston betularia L. Lar,Pic,D,H Poly ? c 1,2 

Bupalus piniarius L. PIN Olig Y+O c 1,3,4 

Deileptenia ribeata Cl. PIN,D Poly ? c 1,3 

Ectropis bistortata Goeze PIN,D,H Poly Y? c 1,3 

Entephria caesiata 

Den. & Schiff. Pin,D,H Poly ? c 1,2 

Eupithecia conterminata Zell. Pic Mono 0? c 2,5 

E. indigata Hb. PIN Olig y c 1,3 

E. intricata Zett. Jun Mono ? c 1,2,5 

E. lanceata Hb. PIN Olig y c 2,3 

E. laricata Fr. Lar,Jun MonoJ Y? c 1,2,3 

E. nanata Hb. PIN,H Poly ? c 1,2,6 

E. pus illata 

Den. & Schiff. PIN Olig Y+O c 2,3,7 

Gymnoscelis rufifasciata Haw. Pic,Pin,D,H Poly ? c 1,2 

Hydriomena furcata Thnbg. Pic,Pin,D,H Poly ? c 1,3 

Hylaea fasciaria L. Pin, (Pic), D Poly 0 c 1,3,8 

Odontopera bidentata Cl. Pin,Abi,H Poly 0 c 1,2,3 

Operophtera brumata L. Pic,D Poly y c 1,2,3 

0. fagata Scharf. Pic,D Poly y c 1,2,3 

Peribatodes secundaria Esp. Pic,Pin Olig (Y)O c 1,3,7 

P~rizoma didymata L. Pic,Pin,H Poly ? c 1,2 

Semiothisa liturata Cl. PIN,Jun OligJ 0 c 1,9,10 

s. signaria Hb. PIN Olig 0 c 1,3 

Thera cognata Thnbg. Jun Mono ? c 1,2 

T. firmata Hb. Pin,Jun MonoJ 0 c 1,3,11 

T. juniperata L. Pic,Jun MonoJ ? c 1,3 

T. obeliscata Hb. PIN,Jun OligJ ? c 1,3 

T. variata 

Den. & Schiff. PIN,Jun OligJ Y+O c 2,3,8 

Lymantriidae 

Lymantria dispar L. Lar,Pin,D,H Pol* y c 1,3,12 

L. monacha L. PIN,D Poly Y+O** c 1,3,12 

Orgyia antiqua L. PIN,D,H Poly Y(O) c 1,2,3 

Noctuidae 

Acronicta rumicis L. Pic,D,H Poly ? c 1,2,13 

15 
APPENDIX B continued 

Family Host Host Tissue Feeding 

Species plants1 range2 age 3 mode4 References 

Blepharita adusta Esp. Pic,Pin,H Poly 0 c 1,13 

Ceramica pisi L. Lar,Pic,D,H Poly ? c 1,3,13 

Panolis flammea 

Den. & Schiff. PIN, (Jun), D Poly Y+O c 1,3,14 

Panthea coenobita Esp. PIN Olig 0 c 2,3,7 

Lasiocampidae 

Dendrolimus pini L. PIN Olig Y+O c 3,15 

Lasiocampa quercus L. PIN,D,H Pol* ? c 1,3 

Macrothylacia rubi L. Pic,D,H Poly ? c 1,2 

Selenephera lunigera Esp. PIN Olig ? c 2,3 

Sphingidae 

Hyloicus pinastri L. PIN Olig ? c 1,3,16 

* Possibly ecological races with respect to host plant choice 

** If on spruce, feeds as young larvae on young tissue and later as old larvae 

on old tissue; if on pine, vice versa 

1 Abi -Abies, Lar - Larix, Pic - Picea, Pin= Pinus, and Jun- Juniper; PIN = 

several spp. within Pinaceae; D indicates that the insect species utilizes one 

or several deciduous trees or bushes; H indicates that it utilizes one or 

several herbaceous plant species. 

2 Mono - monophagous, Olig = oligophagous, OligJ - feeding on some member of 

Pinaceae and Juniper, and Poly= polyphagous. 

3 Y - young tissue (buds and current-year needles) and 0 = old tissue 

(one-year-old or older needles). 

4 C- chewing, M =mining in needles, BM =mining in buds (and/or shoots). 

Arrows under Tissue-age and Feeding mode indicate that the insect shifts from 

~y when it becomes older. 

REFERENCES: 1) Winter (1983), 2) Nordstrom et al. (1941), 3) Schwenke (1978), 

4) Engel (1939), 5) Hoffmeyer (1966), 6) Browne (1968), 7) Patocka (1960), 

8) Escherich (1931), 9) Schwenke (1953), 10) Hofmann (1941), 11) Larsson and 

Tenow (1980), 12) Tr~gardh (1939), 13) Forster and Wohlfahrt (1971), 

14) Schwerdtfeger (1970), 15) Gronberg (1903), and 16) Nunberg (1939). 

16 
APPENDIX C 

Host-plant utilization, host range, utilized tissue-age, and feeding mode of 

Hymenoptera, Symphyta feeding on Swedish conifers. Information on the 

occurrence of individual species in Sweden was taken from Hedqvist (pers. 

comm.). 

Family Host Host Tissue Feeding 

Species plants1 range2 age3 mode4 References 

Pamphiliidae 

Acantholyda erythrocephala L. Pin Mono (Y)O c 1,2 

A. flaviceps Retz. Pin Mono Y+O c 2 

A. posticalis Mats. Pin Mono Y+O* c 1,2 

Cephalcia abietis L. Pic Mono (Y)O c 2 

c. arvensis Panzer Pic Mono Y-+0 c 2 

c. erythrogastra Htg. Pic Mono Y+O c 3 

c. falleni Dalm. Pic Mono Y+O c 2 

Diprionidae 

Diprion butovitschi Hedqv. Pin Mono Y+O c 2,3 

D. pini L. Pin Mono Y-+0 c 1,2,4 

D. simile Htg. Pin Mono Y+O c 1,2,5 

Gilpinia frutetorum F. Pin Mono Y+O c 1,2,4 

G. hercyniae Htg. Pic Mono (Y)O c 1,2 

G. pallida Klug Pin Mono Y+O c 1,2 

G. verticalis Guss. Pin Mono Y+O c 2,6 

G. virens Klug Pin Mono Y+O c 1,2 

Hicrodiprion pallipes Fall. Pin Mono Y+O c 1,2,7 

Honoctenus juniperi L. Jun Mono Y+O c 1,2 

H. obscuratus Htg. Jun Mono Y+O c 2 

H. subconstrictus Thoms. Jun Mono Y+O c 2 

Neodiprion sertifer Pin Mono 0 c 1,2,4 

Tenthredinidae 

Pachynematus montanus Zadd. Pic Mono Y-+0 c 1,2 

P. scutellatus Htg. Pic Mono Y-+0 c 1,2 

Pristiphora abietina Christ. Pic Mono Y+O c 1,2 

P. ambigua Fall. Pic Mono Y+O c 1,2 

P. amphibola Forst. Pic Mono Y+O c 1,2 

P. compressa Htg. Pic Mono Y-+0 c 1,2 

P. saxesenii Htg. Pic Mono Y-+0 c 1,2 

P. subarctica Forssl. Pic Mono Y+O c 1,2 

* Two forms, one feeding on young tissue and the other on old tissue 

17 
1 Abi =Abies, Lar = Larix, Pic = Picea, Pin- Pinus, and Jun = Juniper; PIN= 

several spp. within Pinaceae; D indicates that the insect species utilizes one 

or several deciduous trees or bushes; H indicates that it utilizes one or 

several herbaceous plant species. 

2 Mono = monophagous, Olig = oligophagous, OligJ = feeding on some member of 

Pinaceae and Juniper, and Poly - polyphagous. 

3 Y - young tissue (buds and current-year needles) and 0 

(one-year-old or older needles). 

old tissue 

4 C =chewing, M =mining in needles, BM mining in buds (and/or shoots). 

Arrows under Tissue-age and Feeding mode indicate that the insect shifts from 

~y when it becomes older. 

REFERENCES: 1) Winter (1983), 2) Schwenke (1982), 3) Hedqvist (pers. comm.), 

4) Escherich (1931, 1942) 5) Monro (1935), 6) Hedqvist (1972), and 7) Eidmann 

and Klingstrom (1976). 

18 
APPENDIX D 

Host-plant utilization, host range, utilized tissue-age, and feeding mode of 

Coleoptera feeding on Swedish conifers. Information on the occurrence of 

individual species in Sweden was taken from Ehnstrom (pers. comm.). 

Family Host Host Tissue Feeding 

Species plantsl range2 age3 mode4 References 

SPECIES IN WHICH LARVAE FEED ON NEEDLES AND/OR BUDS 

Anobiidae 

Dryophilus pusillus Gyll. PIN Olig y c 1,2 

Curculionidae 

Anthonomus phyllocola Hrbst. Pin, (Pic) Olig Y? c 1,2 

A. pinivorax Silfverb. Pic,Pin Olig y c 1,2 

Brachonyx pineti Payk. Pin Mono ? c 1,2 

SPECIES IN WHICH IMAGINES FEED ON NEEDLES AND/OR BUDS 

Scarabaeidae 

Amphimallom solstitiale L. Pin,D Poly ? c 2 

Cerambycidae 

Monochamus galloprovoncialis 01. Pin, (Pic) Olig ? c 1,2,3 

M. sutor L. Pic,Pin Olig ? c 1,2 

Chrysomelidae 

Calomicrus pinicola Duft. Pin, (PIN) Olig 0 c 1,2 

Cryptocephalus pini L. PIN, (Jun) OligJ Y? c 1,2 

c. quadripustulatus Gyll. PIN Olig ? c 1,2 

Syneta betulae F. Pic,D Poly y c 1,2 

Curculionidae 

Anthonomus phyllocola Hrbst. Pin, (Pic) Olig ? c 1,2 

A. pinivorax Silfverb. Pic,Pin Olig Y? c 1,2 

Brachonyx pineti Payk. Pin Mono ? c 1,2 

Brachyderes incanus L. Pin Mono ? c 1,2 

Otiorrhyncus leoidopterus F. PIN Olig ? c 1,2 

0. nodosus Mull. Pin Mon? ? c 1 

0. scaber L. PIN Olig ? c 2 

0. singularis L. PIN,D,H Poly Y(O?) c 2,4 

Philopedon plagiatum Schall. Pin,Pic,D,H Poly ? c 1 

Strophosoma capitatum de G. Pin,Pic,D,H Poly ? c 1 

S. melanogrammum Forst. Pin,Pic,D,H Poly ? c 1 

19 
1 Abi -Abies, Lar -Larix, Pic - Picea, Pin- Pinus, and Jun- Juniper; PIN -

several spp. within Pinaceae; D indicates that the insect species utilizes one 

or several deciduous trees or bushes; H indicates that it utilizes one or 

several herbaceous plant species. 

2 Mono - monophagous, Olig - oligophagous, OligJ - feeding on some member of 

Pinaceae and Juniper, and Poly - polyphagous. 

3 Y - young tissue (buds and current-year needles) and 0 

(one-year-old or older needles). 

old tissue 

4 C- chewing, M- mining in needles, BM- mining in buds (andjor shoots). 

Arrows under Tissue-age and Feeding mode indicate that the insect shifts from 

~y when it becomes older. 

REFERENCES: 1) Ehnstrom (pers. comm.), 2) Schwenke (1974), 3) Hellrigl (1971), 

and 4) Browne (1968). 

20 
SAWFLIES AND PONDEROSA PINE: 

HYPOTHETICAL RESPONSE SURFACES 

FOR PINE GENOTYPE, ONTOGENIC STAGE, 

AND STRESS LEVEL 

MICHAEL R. WAGNER 

School of Forestry 

Box 4098, Northern Arizona University 

Flagstaff, AZ 86011 U.S.A 

INTRODUCTION 

Patterns that occur in nature are the result of a complex set of current and historical factors 

that interact with one another and the adaptive plasticity of plants. Scientists are forced to assess such 

processes ·on the basis of series of "snapshots" over a relatively short time that represent only part of 

the grand pattern. In the case of insects interacting with forest trees, there are dozens of 

environmental and host plant factors that could be the key factor responsible for the patterns we 

observe. Because of the high experimental standards of research and the many potentially important 

factors, scientists tend to construct models by which to test specific hypotheses about key factors. This 

methodology produces a body of knowledge about a particular factor (e.g. moisture stress) that does 

not neCessarily integrate well with the body of knowledge about a second factor (e.g. genetic 

resistance). These disjoint sets of data encourage scientists to think in terms of components, and that 

leads them to draw conclusions about single factors, in isolation from many other important factors. 

Such conclusions can be misleading. 

Given the single-factor focus of the scientific community, it is not surprising that inconsistencies 

and apparent contradictions are abundant. For example, despite considerable research effort, no clear 

pattern has emerged to determine the role of environmental stress in creating insect outbreaks (Larsson 

1989). Drought or poor site conditions have been correlated with outbreaks of forest insects (Mattson 

and Haack 1987a, 1987b ). In the specific case of sawflies (Hymenoptera: Diprionidae ), many outbreaks 

have been correlated with drought conditions (Kapler and Benjamin 1960, McLeod 1970, Averill and 

Fowler 1973, Knerer and Atwood 1973, Larsson and Tenow 1984). One hypothesis explaining this 

phenomenon is that environmental stress changes the host plants and thereby increases herbivore 

performance in some way. Tests of this hypothesis for sawflies have not been consistently supportive 

(McCullough and Wagner 1987, Craig et al. 1991, Wagner and Frantz 1990). Meyers (1988) and 

Larsson (1989) have suggested that the general hypothesis that host plant stress causes outbreaks is 

"still very much open to debate." Careful reviews of the literature which stratify the evidence by insect 

feeding guilds clarify the question for some guilds such as bark beetles, but not for others such as 

defoliators (Larsson and Tenow 1984, Larsson 1989). The recent studies cited above might lead us to 

conclude that there is no relationship between stress and insect outbreaks, but what about all the 

previous correlative evidence and the anecdotal evidence that stress ~ related to insect outbreaks? It 

seems reasonable to hypothesize that stress is important under some circumstances and not others. 

The critical point is that several factors interact to create the particular insect/tree pattern we observe 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

21 
at any given moment. When we consider multiple factors simultaneously, we can better define those 

instances in which a factor will or will not be influential. 

In this paper I discuss the general evidence from the literature and my preliminary experimental 

evidence that at least three variables (genotype, ontogeny, and stress) influence the population 

parameters of Neodiprion spp. (Hymenoptera: Diprionidae), which feed on ponderosa pine, Pinus 

ponderosa Dougl. ex Laws. I also present some hypothetical response functions for these single factors. 

Then I generate some three-dimensional figures that illustrate how two individual variables could 

interact to create a response surface. Finally, I illustrate how it is possible to generate from very 

realistic univariate response functions complex response surfaces which could explain otherwise 

apparently contradictory results. 

ROLE OF GENOTYPE IN SAWFLY-PONDEROSA PINE INTERACTION 

For most plants there is a range of natural suitability for insects that appears to be genetically 

controlled. Significant genotype variation in forest trees to insects has been identified for bark beetles 

(Stark 1965, Callaham 1966, Berryman 1972, Smith 1972, Smith 1975), scales and aphids (Hoff and 

McDonald 1977, Mattson et al. 1988), pitch midge (Hoff 1988), pine weevils (Hall 1959, King 1971, 

Wilkinson 1979, Harris et al. 1983, Brooks et al. 1987), shoot moths (Hertel and Benjamin 1975, 

Charles et al. 1982), cone insects (Askew et al. 1985), defoliators (Tigner and Mason 1973, Genys and 

Harman 1976, McDonald 1979, 1982, Fogal et al. 1982), and pine sawflies (Arend et al. 1961, Wilson 

1966, Wright et al. 1967, Henson et al. 1970). Interestingly, Mattson et al. (1988) argue that there is 

relatively little evidence for genetic resistance to free-feeding defoliators. Part of their data is based on 

examination of the susceptibility of trees in range-wide provenance plantations. It may be that the 

procedures used for creating the provenances trials resulted in inadvertent selection of only susceptible 

genotypes. For example, it may be that the provenance collection sites were areas with relatively low 

defoliator pressure and hence a low selection for insect resistance. At any rate, the evidence suggests 

that there is some genotypic variation in insect susceptibility for most tree species. 

For the past 3 years I have been attempting to identify individual trees that exhibit phenotypic 

resistance to pine sawflies. My basic procedure has been to identify unattacked trees within sawfly 

outbreak areas. These phenotypically resistant trees have then been paired with nearby phenotypically 

susceptible trees. To date 10 pairs of trees have been identified. I have bioassayed the trees by caging 

sawflies on them and measuring stage-specific survival. Following Hanover (1975), seed has been 

collected from 14 of the 20 trees and half-sib families have been established. The performance of 

sawflies on the maternal trees of the 14 half-sib families is presented in Fig. 1. Whether the traits 

that influence susceptibility to sawflies in the maternal trees are inherited by the progeny (half-sibs) has 

yet to be determined, but it is clear that there is considerable variation in sawfly resistance in the 

maternal phenotype (2 to 65 percent sawfly survival), and this is an indication of genetic resistance 

(Bingham 1966, McDonald 1979). 

On the basis of the previously cited literature and my preliminary findings, I believe that there 

is substantive genetic variation in ponderosa pine resistance to herbivores. In other words, when all 

other factors are held constant, there can be considerable variation in insect performance based on 

plant genotype alone. For example, I observed a thirtyfold variation in sawfly survival among different 

ponderosa pine individuals (Fig. 1 ). As yet it cannot be established that all of this variation is the 

result of genetic factors, but it is highly probable that some of the variation is due to genetic factors. 

Greater knowledge about the genetic variation of ponderosa pine could greatly clarify our 

understanding of how host plants and herbivores interact. 

22 
-

0 ~ 

-

_J 

<X 

> 

> 

0:: 

:.> 

(/) 

(/) 

Q. 

w 

0 

> _J 

:.> 

L&.. 

2 

0 

a:: 

Q.. 

0 

0 

w 

z R2 R3 R8 R9 R6 R1 RIO R5 59 R4 510 53 52 54 

HALF SIB FAMILY 

Figure 1. Total generational survival of Neodiprion fulviceps on maternal 

ponderosa pine trees from which 14 half-sib families have been established. 

ROLE OF ONTOGENY IN SAWFLY-PONDEROSA PINE INTERACfiONS 

Many plants show age-related changes in susceptibility to attack by specific insects. Some insect 

species attack juvenile trees, such as sawflies on willows (Craig et al. 1986), cynipid wasps on oaks 

(Washburn and Cornell 1981, Frankie and Morgan 1984), and a chrysomelid beetle on cottonwood 

(Kearsley and Whitham 1989). Other insects attack primarily mature trees: budworms (Blais 1958), 

spruce beetles (Schmidt and Frye 1977, Hard 1985), and Pemphigus aphids (Kearsley and Whitham 

1989). Pine sawflies commonly show age-related preferences on their pine hosts (Knight and 

Heikkenen 1980, Coulson and Witter 1984, Wagner et al. 1986) and generally prefer pole-sized or 

smaller trees. 

In 1987 we conducted some preliminary tests of the age-related suitability of ponderosa pine to 

Neodiprion fulviceps (Cresson). Branches were collected from five trees (similar vigor) of six different 

ages (1, 2, 5, 10, 15, and 20 years). One-year-old foliage was bioassayed under laboratory conditions. 

We observed patterns of oviposition (Fig. 2) and survival (Fig. 3) that suggested an effect of tree age. 

Neodiprion fulviceps had highest survival on 15-year-old trees which is within the usual range of tree 

ages where this sawfly species occurs. It is interesting to note that the optimal age for oviposition 

( < 10 years) was not the same as for survival. Because the trees used in this study were of unknown 

genotype and because the sample size was small, these data are tentative. 

23 
90 100 

IX -

. ;·--·~-- -

0 

w 

teo -· 90 (/) 

0 

IX ""'· a. 

-

> 

0 o, _,0-..._ 0 

w 70 , -o 80 (/) t- ' / \ ' , 

(.!) 

(f) 'o---o ', (.!) 

0 w 

a. \ ..J \ <f > 60 \ 70 t- 0 ' 0 

(f) \ t-

(!) 0 LL. 

(.!) 0 

L&J 

60 t50 o- -o Eggs Oviposited z 

L&J 

u 

·-· 0

/o Total Oviposited 

I 0:: 

01 w 

a. 

I I 0 I 

2 5 10 15 20 

TREE AGE 

Figure 2. Influence of tree age on the number of eggs laid and the percent of 

total female fecundity oviposited for Neodiprion fulviceps on 1-year-old 

foliage of six different ages of ponderosa pine. 

On the basis of the literature and the preliminary evidence collected, I hypothesize that for any 

given sawfly species there is a tree age at which sawfly survival would be optimal. The preferred tree 

age could vary among sawfly species on the same host. This could indicate a method by which sawfly 

species with similar life cycles partition their food resources to avoid competition. A hypothetical 

response function for the relationship between sawfly survival and tree age is presented for three 

ponderosa pine-feeding sawflies (Fig. 4). In this case Neodiprion gillettei (Rohwer), which occurs in 

nature on seedlings, would probably have optimal survival on young trees. In contrast, Neodiprion 

fulviceps, which occurs on much older trees in nature, would probably have optimal survival on older 

trees. I assume that both species' survival response to tree age approximates a normal curve. 

The critical point here is that sawfly survival probably depends on tree age independent of other 

factors. It is possible that an experimental bioassay of a highly resistant and highly susceptible 

ponderosa pine genotype, above or below the acceptable age range for a particular sawfly species might 

indicate that there was no genetic effect, whereas the identical bioassay at the optimal age would 

indicate a clear difference in performance between genotypes. Any insect-plant interaction experiments 

conducted with plant material of an inappropriate age might produce very misleading results. 

24 
1.00 ·-· Egg 

0.90 ·---· Larval 

0.80 ••••••• Total 

- 0.70 

0 ~ , • \ 

- • , ., 0.60 / "'· , 

, \ 

...J , 

<X I \ 

> 0.50 , 

> 0.40 

~- a:: 

::::> 

(/) • 0.30 , 

, 

, 

0.20 ~ ~ . ·. \ 

, . •·. ·. \ 

·----· . . . . . ·. \. • 

. . 0.10 •••• ••••••••••• ·. \ 

. \ . 

. 0 

2 5 10 15 20 

TREE AGE 

Figure 3. Influence of tree age on egg, larval, and total survival of 

Neodiprion fulviceps. 

ROLE OF STRESS IN PINE SAWFLY-PONDEROSA PINE INTERACTIONS 

There is yet no clear consensus on the role of environmental stress in ·provoking insect 

outbreaks even for a single-model system. After 5 years of experimentally stressing ponderosa pine 

under field conditions, we still have not established a clear pattern of stress effect (McCullough and 

Wagner 1987, Wagner and Frantz 1990, Craig et al. 1991). Larvae performed more poorly on stressed 

trees than on controls for most years. However, we have observed that increasing stress caused 

increased, then decreased sawfly performance at some period during the 5-year study. This suggests 

that there is some stress level for the plant at which insect performance is optimal and above or below 

which performance declines. Because our studies are on wild populations of unknown genotype and 

because the environmental conditions are not uniform between years, our data are inconclusive. Only 

rigorous, highly controlled experimental testing will reveal the true nature of the response function for 

sawfly survival as a result of ponderosa pine stress. In one of the most rigorous studies of waterstress effects on herbivores, English-Loeb (1989) measured a nonlinear population response by the 

25 
_J 

<t 

> 

> 

a:: 

:::::> 

(/) 

>-

_J 

u.. 

3: 

<t 

(/) 

100 

Neod iprion 

gillettei 

Neodiprion 

autumnal is 

Neodiprion 

fulvicep.!_ 

0~-------------------------------------------------------------------- Seedling Pole Sawtimber Mature 

TREE AGE 

Figure 4. Hypothetical response functions for the effect of tree age on the 

survival of three species of pine sawflies that feed on ponderosa pine. 

two-spotted spider mite, Tetranychus urticae Koch, to a range of water-stress levels of its host plant. 

The response was a modified cosine function in which, as stress increased, mite performance first 

declined, then increased to an optimum, and then declined again. 

Considerably more data are required before a complete response function can be presented for 

the effect of ponderosa pine stress on pine sawfly performance. However, it is possible to suggest 

some shapes that response functions may take (Fig. 5). The three hypothetical response functions 

presented in Fig. 5 represent a range of relationships, any one of which might be the real one. The 

shape of that function can have profound effects on the interpretation of experimental results, as I will 

show in the next section. 

26 
...J 

<l 

> 

> 

a: 

:::::> 

(f) 

>- ...J 

lL 

3: 

<l 

(f) 

Low 

STRESS 

Linear 

--Modified Cosine 

(English- Loeb 1989) 

Normal 

High 

Figure 5. Three hypothetical response functions for the relationship between 

sawfly survival and the stress level of ponderosa pine. 

RESPONSE SURFACES FOR HYPOTHETICAL RESPONSE FUNCTIONS 

Up to this point, I have attempted to identify reasonable single-factor response functions for the 

effects of genotype, ontogeny, and drought stress on pine sawfly performance. In this section I present 

some reasonable response surfaces of two factors in combination and illustrate how they might 

influence sawfly survival. 

Six hypothetical response surfaces are presented in Fig. 6. In each of the six cases, I have 

assumed that resistance is a linear function of genotype as approximated by the slope created by the 

bars in Fig. 1. While holding the genetic resistance factor constant, I have plotted the effect of tree 

age based on the hypothetical response functions presented in Fig. 4 (Fig. 6a, b, c) and the effect of 

stress based on the hypothetical response functions presented in Fig. 5 (Fig. 6d, e, f). 

In examining the effect of tree age across a range of genotypes, one finds several interesting 

patterns emerging. First, sawfly survival can vary dramatically for a given tree age and sawfly species 

depending on the host genotype. The optimal age of ponderosa pine for N. gillettei on a resistant 

genotype would result in less than 50 percent survival, for example, whereas on a susceptible genotype, 

survival would be 100 percent (Fig. 6a). Likewise for a given genotype and sawfly species, sawfly 

survival can vary dramatically as a function of tree age. In the case of N. autumnalis Smith (Fig. 6b), 

survival on a susceptible genotype at the preferred age would be 100 percent, but survival on the same 

susceptible genotype at the least preferred age would be only about 50 percent. If an experimental 

system does not have control over both of these variables, it is possible to generate experimental data 

that demonstrate an infinite array of responses for sawfly performance as a function of tree age. 

27 
A • MOOEL• Genetic • linnr 

TrN Age • normal 

Preference for seedlings e.9. !:!.: g!.l!.!!!.!i 

C • MOOEL• Genetic • linear 

E.MOOEL• 

.J 

<l 

~ 

> 

a: 

::) 

Cl) 

~ 

"'" 

~ ~ Cl) 

I 

I 

I 

0 L 

Low 

Tr .. Age • 110rmal 

Preference for old treu e.g. !:!.: !!!lri.E!P.! 

Gene lie • linear 

Slrtll • 110rmal 

High 

B . MOOEL• Genetic • linear 

Tree Age • normal 

Preference for middle ove trees e.Q. !:!.: ~ 

.J 

<l 

> 

> 

a: 

::) 

Ill 

>- .J 

"'" ~ 

<l 

Ill 

D. MOOEL• Genetic • lineor 

100 

F. MOOEL• Genetic • lineor 

Strus • modified cosine 

.J 

<l 

~ 

> 

a: 

::) 

Ill 

>-

.J 

"'" ~ 

<l 

Ill 

High Low 

Figure 6. Hypothetical response surfaces for the effects of ponderosa pine 

genotype, tree age, and stress on the survival of pine sawflies. Response 

surfaces assume that the effects of tree age and stress are independent of 

genotype. 

28 
Similarly, tree stress can result in widely different effects depending on the tree genotype. Even 

in the simplest case, when the effects of stress and genotype are linear (Fig. 6d), it is still possible to 

obtain highly variable responses if either genotype or stress is not carefully controlled. In the most 

complicated case, when resistance is linear and stress is a modified cosine function (Fig. 6t), it is 

possible to observe an increase or decrease in sawfly survival with increasing stress depending on the 

initial level of stress. Finally, it is important to recognize that a wide variety of genotype, age, and 

stress levels could produce the same sawfly survival. A resistant genotype that was highly stressed 

could produce the same degree of sawfly survival as a susceptible genotype that was not stressed. Thus 

examination of response surfaces can greatly facilitate our understanding of these relationships. 

RESPONSE SURFACES AS AN EXPLANATION OF CONTRADICTORY RESULTS 

One of the assumptions I made in generalizing the hypothetical response surfaces in Fig. 6 was 

that the effects of tree age and stress were the same across all genotypes. In other words, I assumed 

that a resistant genotype would have the same response curve to tree age and stress as would a 

susceptible genotype. In fact there is no reason to assume that is so. For example, sawfly survival 

may not increase on a resistant genotype until that genotype is very heavily stressed. Conversely, 

sawfly survival might increase quickly with low-level stress on a susceptible genotype, but drop 

drastically at moderate to high levels of stress. 

I have illustrated the potential effects of variable response functions across genotypes in Fig. 7. 

In this case I create slightly different response functions for susceptible and resistant genotypes. It is 

possible to observe (Fig. 7, large stress arrow) quite variable effects of an increase in stress at different 

specified stress levels. For genotype A, an increase in stress results in a decrease in sawfly survival, 

whereas for genotype B, an increase in stress results in an increase in survival. Likewise for a specific 

genotype (Fig. 7, large genotype arrow), sawfly survival will decrease with an increase in stress at stress 

level A and increase with an increase in stress at stress level B. It becomes obvious with examination 

of Fig. 7 that all of the hypothetical response functions presented for the effect of stress in Fig. 5 

could be contained in a single complex response surface. The contradictory results reported in the 

literature and emerging from our own experimental data could be explained by a complex model such 

as that presented in Fig. 7. 

UTILI1Y OF EXAMINING RESPONSE SURFACES 

The purpose of the previous discussion on response surfaces was to demonstrate how reasonable, 

individual variable response functions could be combined to create very complex response surfaces. I 

have discussed only cases involving two factors interacting to influence sawfly survival. We know that 

in nature many more factors interact. I am led to conclude that much more carefully controlled 

experimental work is required before true response surfaces are likely to emerge for any insect-plant 

system and for any two sets of variables. Without a very disciplined approach to the analysis of 

individual factors and combinations of factors, we will probably wander for years generating points on a 

response surface without ever fully recognizing the shape of the overall surface. 

To improve the probability of our discovering the true response surface of host plant variables 

influencing insect survival, I propose the following protocols. 1) Research should focus on single 

insect/host models. Only long-term attention to key host plant traits can identify true response 

surfaces. 2) Strongly experimental approaches are required which attempt to hold as many factors 

constant as possible while testing for the factor of interest. Common garden/field, greenhouse, or 

laboratory studies are more productive than natural field studies in which many variables are not 

controlled. 3) Experiments on single factors such as stress must test across the full range of that 

factor. As Figs. 6 and 7 demonstrate, an increase in stress could lead to quite variable effects on 

survival depending on the initial stress level. 4) Multifactor experiments are useful only when the 

29 
MODEL Genetic = linear 

Stress = modified cosine 

100 Stress Level 

A 

\~ ~~ 

~~ss 

s~ \ 

Stress A t Stress B f 

Figure 7. Hypothetical response function for the effects of genotype and 

stress on sawfly survival. Model assumes the stress response function is 

dependent on genotype. 

individual factors are thoroughly understood. 5) Insect response variables need to be chosen carefully. 

The response variable chosen (e.g. total survival) should be one that can have a significant effect on 

insect population dynamics. Field data and population dynamics models can be helpful in identifying 

which population parameters are most important for a given insect/plant system. 6) We should be very 

careful about generalizing across insect and plant systems. What may be a key factor in one system 

may be unimportant in another. Observation of natural patterns will suggest which factors are most 

likely to be important for a given system and these should be explored first. 7) Finally, response 

surfaces must be carefully defined. As this paper has attempted to demonstrate, relatively simple 

single-factor response functions, when combined, can produce complicated response surfaces which must 

be understood before definitive conclusions can be drawn. 

30 
SUMMARY 

In this paper I have reviewed the general literature and examined preliminary data that implicate 

genotype, ontogeny, and stress as host factors that influence survival of pine sawflies on ponderosa 

pine. Data and the literature have been used to generate hypothetical single-factor response functions. 

These response functions have been combined to create response surfaces illustrating the potentially 

complex nature of response surfaces derived from relatively simple response functions. Finally I 

propose some research protocols to ensure efficient methods of generating response surfaces in order 

to establish clear relationships between host plants and their insect herbivores. 

ACKNOWLEDGMENTS 

I would like to thank Zhao-Yi Zhang for assistance in collecting preliminary data on the effect 

of tree age on sawfly survival. I would also like to thank Karen M. Clancy, Clarence S. Dunbar, and 

Joel D. McMillin for reviewing the manuscript. D.P. Dykstra and T.E. Gross provided valuable 

assistance in generating the three-dimensional figures. 

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31 
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32 
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33 
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34 
DOES REPRODUCfiON COMPROMISE DEFENSE 

IN WOODY PLANTS? 

DANIEL A. HERMS and WILLIAM J. MATTSON 

The Dow Gardens 

1018 W. Main St., Midland, MI 48640 U.S.A 

and 

Department of Entomology 

Pesticide Research Center, Michigan State University 

East Lansing, MI 48824 U.S.A 

USDA Forest Service 

North Central Forest Experiment Station 

1407 S. Harrison Road, East Lansing, MI 48823 U.S.A 

and 

Department of Entomology 

Pesticide Research Center, Michigan State University 

East Lansing, MI 48824 U.S.A 

PRINCIPLES OF RESOURCE ALLOCATION 

A general principle of adaptive allocation was proposed by Cody (1966) who hypothesized that 

1) all living organisms have finite resources to partition among growth and competing physiological 

processes such as reproduction and defense; and 2) natural selection results in the evolution of unique 

resource allocation patterns that maximize fitness in different environments. Today, it is well 

established that plants have limited resources to allocate among these processes (Bazzaz et al. 1987), 

and theories of life-history strategy rests on the assumption that there are fitness trade-offs associated 

with varying patterns of resource allocation (Steams 1976, 1989, Reznick 1985, Bazzaz et al. 1987, 

Lovett Doust 1989). Trade-offs occur when an increase in resources allocated to one fitness 

component, such as growth, reduces the allocation to another, such as reproduction. Natural selection 

(acting within phylogenetic, physiological, and ecological constraints) should shape patterns of resource 

allocation, balancing the costs and benefits associated with these trade-offs, resulting in the evolution of 

life-history strategies maximizing fitness. There are direct and indirect costs associated with allocation 

to "nongrowth" processes such as reproduction. Direct costs are energy and assimilates invested in 

reproductive structures. Indirect costs are unrealized growth and future reproduction as a result of this 

investment (Bazzaz and Reekie 1985, Bloom et al. 1985, Bazzaz et al. 1987, Reekie and Bazzaz 1987c, 

Ronsheim 1988, Lovett Doust 1989). 

The physiological cost of reproduction in the form of reduced vegetative growth has been 

documented in a number of cases (Gross 1972, Harper and White 1974, Gifford and Evans 1981, 

Willson 1983, Luken 1987, Clark and Clark 1988, Snow and Whigham 1989, Dick et al. 1990). 

However, this cost may not be universal (Tuomi et al. 1982, Reekie and Bazzaz 1987c, Remick 1985). 

Genetic, ecological, and physiological trade-offs between growth and defensive secondary chemistry are 

also well documented (Bryant et al. 1983, Krischik and Denno 1983, Coley et al. 1985, Loehle 1988, 

Bazzaz et al. 1987, Pimentel 1988). Resource allocation patterns are the expression of source-sink 

BARANCHIKOV, Y.N., MA'ITSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

35 
interactions within the plant and their control on assimilate partitioning. Complex physiological 

changes in patterns of assimilate partitioning are required to bring about the maturation of 

inflorescences, fruits, and seeds. Very likely, these changes will affect traits conferring plants with 

resistance to herbivores. Few studies, however, have examined the potential interactions between 

reproduction and defense. 

In this paper we explore two hypotheses suggesting how plant reproduction may directly and 

indirectly affect herbivory and review the limited experimental evidence supporting each: 

1) reproductive structures as carbon sinks reduce the allocation of resources to defense; 2) reproductive 

structures as nutrient sinks increase the carbon/nutrient ratio in nearby vegetative tissues, resulting in 

their increased secondary metabolism and consequent increased resistance to herbivores. 

TRADE-OFFS BETWEEN REPRODUCTION AND DEFENSE 

Plants have limited resources to support their physiological processes, hence all requirements can 

not be met simultaneously, and trade-offs occur among growth, maintenance, storage, reproduction, and 

defense processes. Consequently, there is sequential growth and maturation of tissues within organs 

and organs within plants and/or strong inverse relationships between the allocation of resources to 

growth and nongrowth processes, including reproduction and defense (Mooney 1972, Mooney and Chu 

1974, Gifford et al. 1984, Bloom et al. 1985, Willson 1983, Krischik and Denno 1983, Coley et al. 

1985, Alpert et al. 1985, Loehle 1988, McLaughlin and McConathy 1979, Bazzaz et al. 1987, Patrick 

1988). 

Though rarely documented, reproductive effort may come at the expense of defense, if resources 

are diverted from resistance mechanisms to reproductive structures. This may occur commonly in the 

case of nitrogen-based secondary metabolites such as alkaloids and cyanogens, the concentrations of 

which often decline in foliage as growth shifts from vegetative to reproductive processes (Mattson 1980, 

Krischik and Denno 1983, Harborne 1990). 

Resistance of conifers to bark beetles is generally correlated with their growth efficiency, 

i.e. stemwood production per unit foliage (Waring et al. 1980, Waring 1983, Mitchell et al. 1983, 

Larsson et al. 1983, Waring and Pitman 1985). Susceptible individuals with low growth efficiencies are 

characterized by depleted levels of the stored energy necessary to support defensive reactions (Waring 

and Schlesinger 1986, Christiansen et al. 1987). Because heavy pollen and cone production can reduce 

growth efficiency, episodes of reproduction may increase susceptibility to bark beetles. For example, 

cone production has been shown to depress stem-wood growth and leaf area in several species of 

conifers (Eis et al. 1965, Owens 1969, Tappeiner 1969, Dick et al. 1990). Carbon allocated to 

reproduction at the expense of energy and substrate required for resin synthesis and wound-induced 

hypersensitive responses may contribute to increased bark beetle and pathogen susceptibility. 

Reproductive effort may interact with environmental stress to suppress conifer resistance to bark 

beetles and contribute synergistically to outbreaks. 

Birch Reproduction and Resistance to Bronze Birch Borer 

The pistillate catkins of Betula are known to be strong photosynthetic sinks, competing with and 

reducing resource allocation to vegetative growth (Gross 1972, Tuomi et al. 1982, Caesar and 

MacDonald 1983). Frequently trees producing especially heavy seed crops subsequently exhibit severe 

dieback symptoms (Gross 1972, Houston 1987). 

Our studies into the physiology of birch resistance to bronze birch borer suggest there may be a 

direct trade-off between female reproductive effort and resistance to the bronze birch borer (Agri.lus 

anxius). Bronze birch borer larvae feed under the bark on the xylem-cambium-phloem interface and 

36 
are restricted to feeding upon living tissue. Feeding girdles the tree, disrupting the downward transport 

of photoassimilates. Dieback of roots occur as they are isolated from their energy source, thereby 

limiting nutrient and water uptake. As attack intensifies, dieback initiates and spreads within the 

canopy. Heavily infested trees are invariably killed (Anderson 1944, Barter 1957, Carlson and Knight 

1969). 

From 1986 to 1989, we conducted a controlled, factorial, field experiment investigating the 

effects of soil moisture, soil fertility, and defoliation on the expression of birch resistance to bronze 

birch borer. We found soil moisture to be the most important environmental variable affecting 

resistance. Water deficit reduced rates of photosynthesis, growth, and wound-callus formation, as well 

as resistance to bronze birch borer (Herms and Mattson, unpubl. data). We found that paper birch 

resistance to bronze birch may be based largely on generalized trunk responses to wounding, especially 

rapid wound-callus formation. Furthermore, we found that the strength of this response is dependent 

on an adequate supply of available current photosynthate (Herms and Mattson, unpubl. data). 

Feeding-wounds stimulate callus formation, which if rapid enough, may entirely encapsulate small larvae 

within suberized tissue containing high concentrations of secondary chemicals and low concentrations of 

nutrients. Normally xylem tissue is a poor source of nutrition (Haack and Slansky 1987); callus tissue 

may be even worse, preventing larvae from completing development. Larvae may also be physically 

crushed as they are overgrown by callus. In effect, larvae may be in a developmental race against the 

tree. Larvae move through the tree in essentially two-dimensional space as they feed, their rate of 

progress correlated with their rate of consumption. Lesion development characteristic of a 

hypersensitive response occurs in phloem and xylem tissue surrounding the wound. A rapid rate of 

callus formation, coupled with reduced rates of larval movement through the wood, may result in larval 

encapsulation. Implicit in this hypothesis is the prediction that the rate of callus formation necessary 

for resistance should be presented by a threshold value approximately equal to the maximum rate of 

larval movement through the plant. Our data suggest that birch trees with rates of callus formation 

falling below about 0.02 mm/day are highly susceptible to bronze birch borer. 

Paper birch (Betula papyrifera) is monoecious, with pistillate (female) and staminate (male) 

catkins produced as separate structures. Male catkins are produced at the end of indeterminate longshoots in mid- to late-summer following the termination of shoot elongation. They overwinter, 

elongating and releasing pollen as vegetative buds open in spring. Female inflorescences emerge from 

overwintering-buds on short shoots as buds break in spring. Female catkin maturation commences 

upon pollination, and continues throughout the growing season. Seeds mature in late summer and 

drop throughout the fall and winter. 

The results of our experiments confirm previous reports showing a trade-off between vegetative 

growth and female catkin production (Gross 1972, Tuomi et al. 1982, Caesar and MacDonald 1983). 

Plants capable of altering the balance of resources allocated between male and female organs generally 

allocate proportionally more resources to female functions in high resource environments (Freeman et 

al. 1980). This occurs, presumably, because successful female reproduction requires, in general, a 

greater commitment of resources than does male reproduction. In our experiment, however, increased 

female reproductive output in 1 year was associated with resource-limited growth during the previous 

year. Slow growth may stimulate the initiation of female flowers. Female reproduction itself then 

further reduces vegetative growth through resource competition. A positive feedback loop may result. 

Female reproductive effort stimulated by slow growth further reduces growth, which further stimulates 

female reproduction. Because of reduced rates of callus formation associated with increased female 

reproductive effort, this positive feedback loop may result in ever-increasing susceptibility to bronze 

birch borer and eventual tree death. In fact, stress-triggered seed production may be an adaptation 

which maximizes the life-time reproduction of suppressed trees that are competitively doomed and are 

likely to be soon killed by bronze birch borer. 

37 
Another Look at Birch Dieback: Bronze Birch Borer is Central 

Some students of forest decline in North America have been reluctant to assign the bronze birch 

borer a central role in the occurrence of widespread birch dieback (Anderson 1944, Hawboldt 1947, 

Carlson and Knight 1969, Houston 1987). At best, the bronze birch borer has been credited with a 

minor effect on over-all patterns of tree mortality, primarily killing trees already predisposed to death 

by other factors, such as disease. We argue that patterns of bronze birch borer outbreaks are in some 

ways analogous to those of the mountain pine beetle, Dendroctonus ponderosae, and are sufficient in 

themselves to contribute significantly to historical patterns of birch dieback in North America: 

1) outbreaks of the bronze birch borer, like those of the mountain pine beetle, can be classified as 

"eruptive" (Berryman and Stark 1985), or more specifically "pulse eruptive" (Berryman 1987); 2) much 

like the mountain pine beetle (Raffa and Berryman 1983, 1987, Berryman and Stark 1985), we argue 

that bronze birch borer populations are usually regulated largely by the availability of host plants 

suitable for larval development and survival (e.g. Carlson and Knight 1969). Outbreaks occur at 

irregular intervals when biotic and/or abiotic stress factors increase the availability of suitable host 

trees. 3) Once populations reach epidemic proportions, the outbreak spreads to adjacent stands as 

large numbers of larvae are able to overwhelm the defenses of vigorous, normally resistant trees. 

Paper birch frequently forms even-aged, monospecific stands throughout the boreal forest of 

North America. Under conditions favoring rapid tree growth, populations of bronze birch borer are 

constrained to endemic levels by lack of susceptible host material. In this situation, birch borer 

reproduction is primarily restricted to suppressed trees succumbing to density-dependent competition 

during the thinning phase of stand establishment. Intolerant of shade, suppressed trees are 

characterized by low net assimilation rates and lack the resources necessary to support a strong wound 

response. 

Episodes of birch dieback, and associated out-breaks of bronze birch borer, have corresponded 

with periods of above-average temperatures and below-average precipitation (Hawboldt and Skolko 

1948, Redmond 1955, Clark and Barter 1958). Combinations of severe stresses such as drought and 

defoliation may simultaneously weaken trees over wide geographic areas, resulting in rapid and 

substantial increases in host material suitable for the bronze birch borer, thereby releasing them from 

this constraint on population growth (Carlson and Knight 1969). 

Female reproduction in birch may play a key role in sustaining bronze birch borer outbreaks. If 

stress-induced reductions in growth stimulates female reproduction, and female reproductive effort 

further compromises resistance to bronze birch borer, the result may be a positive feedback loop which 

rapidly increases the number of susceptible hosts, intensifying and sustaining an outbreak. 

Under conditions of extremely high attack density, the defense mechanisms of otherwise resistant 

trees may be overwhelmed by simultaneous colonization by many larvae. Under these circumstances, 

larval-feeding behavior may act to subvert host defense mechanisms, facilitating the success of their own 

colonization as well as colonization by other larvae. When feeding in vigorous hosts, larvae display a 

zig-zag pattern of gallery formation as they continually double-back against the grain of the wood 

(Carlson and Knight 1969). This pattern of feeding may partially girdle the tree, causing localized 

reductions in the strength of wound-induced resistance mechanisms. On the other hand, in severely 

stressed host trees, galleries show no consistent pattern, as larvae apparently feed on the freshest 

phloem they encounter (Carlson and Knight 1969). 

As borers kill susceptible trees, thereby removing them from the pool of suitable hosts, and as 

environmental conditions change favoring increased tree growth and stronger wound responses, the 

epidemic subsides. The borer population declines to an endemic level as the supply of suitable hosts 

dwindles. 

38 
Birch trees experiencing traumatic trunk and canopy death frequently maintain sufficient stored 

reserves to resprout from the roots. Substantial resprouting often follows above-ground mortality 

resulting from fire or snowshoe hare browsing. Higher levels of terpenoid surface resins of the bark of 

juvenile growth originating from root-sprouts are toxic to snowshoe hares and may contribute to the 

decline of hare population outbreaks (Bryant 1981, Fox and Bryant 1984). Trees killed by bronze birch 

borer can resprout, as well, and sprouts may be too small to permit bronze birch borer colonization 

for several years. Sprouting following trunk death is obviously an adaptation to catastrophic 

disturbances such as fire and herbivore outbreaks, contributing to the continued dominance by birch of 

seral sites. 

Sexual Variation in Resistance and the Carbon/Nutrient Balance 

Dioecious plants frequently exhibit sexual dimorphism in resources allocated to reproductive 

effort, with female effort generally greatest because of resources required for seed and fruit maturation 

(Lloyd and Webb 1977, Wallace and Rundel 1979, Hoffmann and Alliende 1984, Bullock 1984, Clark 

and Clark 1988, Snow and Whigham 1989, Allen and Antos 1988). Several studies have documented 

intraspecific sexual variation in the degree of herbivory experienced by dioecious plants (Dannen et al. 

1985, Lovett Doust and Lovett Doust 1985, Agren 1987, Elmqvist et al. 1988, Alliende 1989, Boecklen 

et al. 1990). The resource-competition hypothesis predicts increased herbivory on female plants 

because their typically greater reproductive effort competes for resources with defense mechanisms. 

However, data from the few existing studies suggest that the opposite is true. Male plants generally 

experience greater herbivory (Bawa and Opler 1978, Dannen et al. 1985, Agren 1987, Alliende 1989, 

Boecklen et al. 1990). 

Male and female plants may often segregate along environmental gradients (Putwain and Harper 

1972, Freeman et al. 1976, Bawa 1980, Cox 1981, Bierzychudek and Eckart 1988). Differential levels of 

herbivory, possibly resulting in skewed sex-ratios, may arise from 1) differential frequency of herbivore 

encounters in their respective environments, or 2) differential defensive allocations among male and 

female plants. 

The nutrient capital required for the growth, maintenance, and maturation of flowers, fruits, and 

seeds can be substantial and is obtained in full from the rest of the plant (Bazzaz et al. 1979, 

Thompson and Stewart 1981 ). Limiting nutrients may be mobilized in relatively high proportions from 

vegetative tissue to reproductive sinks, thereby contributing to the reductions in vegetative growth 

associated with reproduction (Mooney 1972, Sinclair and de Wit 1975, 1976, Thompson and Stewart 

1981, Bloom et al. 1985, Alpert et al. 1985). The high quantities of nutrients required for fruit and 

seed maturation may contribute to nutrient deficiencies and ensuing growth reductions in female 

relative to male plants (Bullock 1984, Allen and Antos 1988). 

The reproductive structures of many species are photosynthetic, contributing in varying degrees 

to their own economy of energy and biomass (Dickmann and Kozlowski 1970, Bazzaz et al. 1979, 

Reekie and Bazzaz 1987a ). Furthermore, enhanced sink strength associated with rapidly developing 

reproductive structures may stimulate increased photosynthesis in nearby source leaves, through 

feedback mediated effects (Neales and Incoll 1968, Watson and Casper 1984, Foyer 1988, Dick et al. 

1990). As a result, the diversion of carbon from vegetative to reproductive structures may be 

proportionally less than that of nutrients, especially in female plants (Sinclair and de Wit 1975, 1976, 

van Andel and Vera 1977, Lovett Doust 1980, Williams and Bell 1981, Abrahamson and Caswell 1982, 

Mooney and Gulmon 1982, Bullock 1984, Allen and Antos 1988, Reekie and Bazzaz 1987b, Esler et al. 

1989). Biomass alone may not always be a suitable measure of reproductive effort (Thompson and 

Stewart 1981, Abrahamson and Caswell 1982, Bazzaz and Reekie 1985, Reekie and Bazzaz 1987b). 

Rapidly growing tissues are invariably strong photosynthetic sinks (Wareing and Patrick 1975, 

Patrick 1988). However, nutrient limitation slows their growth (Agren 1988, Patrick 1988). 

39 
Photosynthesis, however, can be maintained in existing cells, at nutrient concentrations below those 

limiting to growth (Chapin 1980, Dietz 1989). Under sink-limiting conditions the carbon/nutrient ratio 

of the plant increases. Photosynthate assimilated in excess of growth requirements is frequently 

allocated to secondary metabolism, frequently increasing the plant's resistance to herbivores (Mattson 

1980, Bryant et al. 1983, 1987a, 1987b, Mihaliak et al. 1985, 1987). Since "excess" photosynthates could 

be stored and contribute to future growth rather than be used in defense, enhanced secondary 

metabolism in response to sink limitation may represent a selected, adaptive use of resources 

minimizing herbivory (micro and macro) when the plant has limited ability to compensate (via growth) 

for it. 

A nutrient deficiency in vegetative parts female plants relative to male plants resulting from a 

disproportionate allocation of nutrients from vegetative sources to reproductive sinks may limit 

vegetative growth (Allen and Antos 1988). Photosynthetic stimulation of source leaves by feedback 

control exerted by strong reproductive sinks, coupled with direct photosynthetic activity of reproductive 

tissues, may contribute to a favorable carbon economy within the plant. Together, these factors may 

interact to increase carbon/nutrient ratio in the foliage of female plants relative to males. 

Female plants, because of reduced growth due to their greater reproductive effort, may have 

limited ability to compensate for herbivory relative to male plants (Agren 1987, Elmqvist et al. 1987, 

1988). Limited compensatory ability coupled with the need by female plants to protect their 

reproductive investment, may result in females being under stronger selection than males for powerful 

defense (Putwain and Harper 1972, Agren 1987, Boecklen et al. 1990). Consequently, patterns of 

defense observed in female relative to male individuals of a species may mirror the phenotypic patterns 

of defense predicted by Bryant et al. (1983) in nutrient-deficient relative to nutrient-rich plants. 

Female plants, like nutrient-deficient plants, should display reduced growth, increased carbon/nutrient 

balance in vegetative structures, and higher concentrations of secondary metabolites. Very limited 

evidence supports this pattern. Male plants do seem to receive higher levels of herbivory (Putwain and 

Harper 1972, Dannell et al. 1985, Agren 1987, Elmqvist et al. 1988, Alliende 1989, Boecklen et al. 

1990, Krischik and Denno 1990, Jing and Coley 1990) and contain lower concentrations of secondary 

metabolites or have less tough foliage (Palo 1984, Boecklen et al. 1990). 

Reproductive Effort in Monoecious Plants May Enhance Their Resistance to Folivores 

The principles discussed above should also apply to monoecious plants if they translocate 

proportionally more nutrients than carbon from vegetative sources to reproductive sinks. This 

hypothesis predicts that the carbon/nutrient ratio of vegetative tissues will increase with increasing 

reproductive effort, resulting in increased concentrations of carbon-based secondary metabolites, and 

possibly enhanced resistance to folivores. 

SUMMARY 

The process of plant reproduction has pervasive effects on virtually all aspects of plant 

physiology and should have important effects on plant resistance to herbivores. We hypothesize that 

increased susceptibility to stem-invading herbivores could result as a consequence of the substantial cost 

of reproductive effort as resources are diverted from defensive structures and reactions to reproduction. 

On the other hand, we hypothesize that reproduction can increase plant resistance to folivores. 

Reproductive effort may result in an increased carbon/nutrient ratio in foliage, as nutrients are 

translocated to developing flowers, fruits, and seeds. &sociated with this increased carbon/nutrient 

balance may be enhanced allocation to secondary metabolic pathways and increased resistance to some 

herbivores. Few data are available with which to test these hypotheses. The potential interactions 

between plant reproduction and herbivory are ripe for investigation. 

40 
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46 
PLANT REPRODUCfiVE ORGANS 

AND THE ORIGIN OF TERRESTRIAL INSECfS 

GEORGY V. STADNITSKY 

Technological Institute of Pulp and Paper Industry 

Leningrad 198092 U.S.S.R. 

INTRODUCTION 

It is widely believed that plants facilitated the evolution of terrestrial insects (Southwood 1973). 

However, the mechanisms by which this evolution occurred are not yet fully understood. I therefore 

propose a hypothesis about one possible mode of formation of terrestrial insects and fauna. The soil, 

warm shallow lagoons, tidal zones, and accumulations of detritus are assumed by many authors to be 

the "bridges" for the transition of aquatic organisms to terrestrial existence. 

The linkage of insects to plants has been offered as an explanation for the evolution of 

complete metamorphosis and the ability to fly. It has been suggested that holometabolism occurred in 

narrow cavities of the substrate, which might be represented by the cavities and ducts in the plant 

reproductive organs. It is assumed that wings and the ability to fly evolved owing to its advantages in 

finding food and escaping from enemies. 

The Transit to Land 

The aquatic fauna is known to be extremely diverse; ancestors of the present arthropods were 

highly differentiated in the aquatic environment. In the transient water-land zones, the proto-insect's 

migration onto the land seemed inevitable, although this transit took a long time. Thus it could not 

have been simultaneous for various insect groups, although some groups evolved concurrently. Each 

group probably had its own bridge. Let us imagine those conditions which contributed to an obligatory 

and inevitable transition of aquatic organisms to land. The earth at that time (the Lower 

Silurian-Upper Devonian) was represented mostly by rocky, dry desert with scanty vegetation, oxygen 

deficiency, and unlimited amounts of severe ultraviolet radiation. 

Organisms living in water were shielded from UVR and from drying and over-heating. They 

could easily move in a water environment which provided them with necessary support. Those 

organisms which moved onto land faced formidable ecological difficulties, the most serious being the 

lower viscosity and density of the air as compared to those of the water. Their bodies actually lost 

support and their free movement became impaired. For such groups of ancestral arthropods, soil 

might have been the bridge to terrestrial life. The land was almost devoid of organic life, having 

drastic changes of temperature, humidity, and illumination. The chance to survive and have progeny 

was probably very small. The vegetation (the plant protocommunities) had not yet contributed to the 

process apart from accumulations of detritus and remnants of aquatic plants which served as screens. 

Another, later evolutionary branch of aquatic arthropods was associated with the transition of 

plants to terrestrial existence. This happened as a result of differentiation of the plant life cycle into 

BARANCHIKOV, Y.N., MATI'SON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

47 
sexual (gametophyte) and asexual (sporophyte) generations which was accompanied by the formation of 

a special reproductive organ "strobilus," which may be regarded as an analogue of modern cones. 

Primary-terrestrial plant protocommunities were prostrate creeping plants partly yet connected 

with water, and served as optimal habitat for Arthropoda ancestors to be temporarily found outside the 

water. The reproductive organs rose above the water surface. If we take into account the fact that 

plants in a water environment could have been used as food and shelter by insects, then endophyte 

mode of life could be optimal. Plant fibers on land contained moisture and oxygen, and perhaps the 

reproductive structures provided for the best isolation from external hostile conditions. Moreover, they 

were food substrates rich in nutrients. 

Within this hypothesis it is impossible to imagine other more ecologically optimal habitats for 

the insect's ancestors. Thus we can postulate the existence of two likely "bridges" for the transition 

onto the land of aquatic ancestors; they moved Via the soil and via plant reproductive structures. This 

by no means excludes other ways and means. We should emphasize that these two bridges established 

the two further directions of evolution of terrestrial Arthropoda. The soil bridge Arthropoda actually 

"stopped" their evolution, e.g. the modem Apterygota, Myriapodes, and Arachinoides. Their 

environments excluded both the possibility and the necessity of complete metamorphosis and flying 

ability. The second group has undergone substantial evolution and has transformed into the modern 

Holometabola. We should postulate on the basis of the above that the aquatic ancestors of modem 

insects have not experienced any metamorphosis; this conclusion is recognized by many authors. 

The Origin of Flight 

We can suggest that flight and metamorphosis are inherent features of higher insects and have a 

common origin. They appeared because the association with plants predisposed their evolution. 

Peculiar features of plant reproductive organs, as habitats for endophytes, are their ephemeral, patchy 

existence in comparison with the constant character of the plant proper. They formed on the ends of 

the branches, being unevenly and irregularly distributed depending on dynamic weather and soil 

conditions. In other words, the habitats and food resources of this branch of terrestrial insects 

originally appeared to be discrete in space. Evolution in insects could have proceeded in the following 

way: a certain group of terrestrial insects under certain favorable conditions could make locally a 

morphological and physiological "jump" which can be regarded as aeromorphosis. 

Living conditions in strobilus (or other reproductive organs) were such that an insect as a rule 

could not complete its ontogenesis in one strobilus, it had to move to another one situated nearby, on 

a neighboring branch, or a neighboring plant, the time for migration being extremely limited. Similar 

migrations were performed by adult insects to lay eggs and to provide the food for its progeny. 

Crawling would not have been optimal. A jump would be more advantageous, but jumping makes it 

necessary to overcome gravity and to move large distances. Insects with elongated bodies would be 

favored. The necessity for organs to appear, which would make the insects able to fly first in a passive 

mode and then in an active mode, would be accompanied by re-structuring of muscles and formation of 

a wing. 

Let us now examine a hypothetical fate of an insect grown in the primary plant reproductive 

organ. Its life time was determined by the fulfillment of its own reproduction and was quite short, 

though this does not mean that the whole period of plant reproduction was so short: strobila (or 

other organs) could exist in the tree crowns quite long, new strobilae substituting for old ones. Those 

insects which could deposit their eggs faster had a higher probability to survive and have progeny, 

laying their eggs in the neighboring reproductive organs or in those which died later. Larvae hatched 

from these eggs, that is embryonization of post-embryonal development occurred as postulated by 

Iezhikov-Berleze theory. Under such conditions larvae had to live through unfavorable nutrition and 

development periods (cooling periods, droughts, absence of food and habitats). The development under 

these unfavorable conditions became retarded, but it should have been compensated for by faster rates 

48 
of physiological metabolism (hystolis, histogenesis) in the period of transition from a wingless, sexless 

larva to the winged and sexually mature "imago." 

The development within the living plant tissues did not require the development of 

morphological and physiological adaptation. Exactly the same advantages are available to primary 

wingless insects which occur (and still occur) in strongly moisturized soil cavities. (See Gilyarov 1970.) 

However, the temporal discreteness of plant organs and tissues forced the insect to exist outside plants 

during a certain period of their ontogenesis, which resulted in the forming of new adaptations. The 

development of an isolated pupa (where these processes take place), not affected by the environment, 

appeared to be an optimal evolutionary trend. In a number of cases the developed ability of retarding 

or stopping the development without morphological reconstructions was fixed, i.e. diapause. 

On the other hand, those insects who primarily or secondarily were related to non-discrete plant 

organs (leaves, branches) and have created not only the chewing feeding mode but also a sucking one 

as well (Orthoptera, Heteroptera, Homoptera) did not develop the pupal stage, they are known as 

Hemimetabola. 

The above presents the main concepts of a theory which is by no means complete. It should be 

considered as a preliminary assumption for a future hypothesis. 

49 
PREFERENCE OF DENDROPHAGOUS INSECfS 

FOR FOREST BORDERS 

ANDREY V. GUROV 

V.N. Sukachev Institute of Forest and Wood 

Siberian Branch of the U.S.S.R. Academy of Sciences 

Krasnoyarsk 660036 U.S.S.R. 

INTRODUCfiON 

Numerous investigations have shown that forest insect outbreaks usually occur in specific 

habitats. Frequently these outbreaks do not generally extend to other territories occupied by these 

same host trees. Moreover, in every stand subjected to an outbreak, both slightly undamaged plots and 

heavily damaged plots are found. Perhaps some plots are initially more resistant to insect attack, and 

insect distribution within forest ecosystems may have a mosaic pattern. Therefore investigation of the 

relation between dendrophagous insect distributions and initial heterogeneity of ecosystems may help us 

to understand the nature of forest stand resistance. This question lends interest to the peculiarities of 

dendrophagous insect distribution in relation to forest borders because borders and different glades are 

important factors in forest ecosystem heterogeneity. 

INSECf DISTRIBUTION WITHIN STANDS 

There is no large body of information on this question in the literature. I have used the 

available information on different species from several natural zones and considered the distribution of 

180 species belonging to 33 families of six insect orders. Insect distribution was analyzed only at the 

main feeding stages. 

Table 1 shows the majority (73.3 percent) of the species considered to prefer the forest border 

and its analogues (single growing trees or low-density stands). 

Distribution of insects within a forest stand may depend on two main factors: 1) the presence 

of available food; and 2) microclimatic conditions. It is known that availability of food is more 

important for xylophagous insects than for phyllophagous ones. On the other hand, microclimatic 

conditions are more important for phyllophagous free-living species than for xylophagous ones. Thus it 

is necessary to analyze the distribution of both these insect groups separately. My analysis showed the 

forest border and its analogues to be preferable for the majority of species from both groups: 

59 percent of xylophages and 66 percent of phyllophages. Thus these stations may satisfy different 

requirements (food and climate, among others) of the majority of dendrophages. 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

50 
Table 1. Preferred distribution of 180 phytophagous insect species over 

different forest parts 

Habitats 

Forest borders and their analogues 

Isolated trees (A) 

A+ B 

Forest borders (B) 

B + C 

Open, low-density stands (C) 

A + B + C 

Forest thickets and their analogues 

Closed, high-density stands (D) 

C + D 

Uncertain distribution 

A + B + C + D 

B + C + D 

Uncertain 

Number of species 

Total 

3 

5 

18 

46 

49 

11 

29 

7 

4 

1 

7 

% 

1.7 

2.8 

10.0 

25.6 

27.2 

6.1 

16.1 

3.9 

2.2 

0.5 

Climatic conditions are different in every natural zone, however, and the insect species areas 

may occur over several bioclimatic zones. Therefore dendrophage distribution in relation to forest 

borders may be different. Dispersal from one natural zone to another provide ample evidence that 

insect species exchange one kind of habitat for another. We should take this principle into account in 

our strategies for controlling insect species epidemics, but for our present purposes it is more 

interesting to consider dendrophage distribution within different zones, such as forest and steppe 

regions. 

My data analysis again showed the majority of species to prefer the forest border and its 

analogues: 84 percent the forest zone and 71 percent the steppe. So these "border" habitats are 

assumed to have an advantage over forest thickets and their analogue for insects. 

There is data indicating some abundant species use the forest borders as a refuge between 

outbreaks. Moreover, the initial outbreak areas often coincide with these refugia. At the same time, 

my analysis showed both outbreak and nonoutbreak insect species (81 percent and 79 percent 

respectively) to prefer forest borders. We may say, then, forest borders not only function as refuges 

for abundant species, but are preferred habitats for the majority of nonoutbreak species as well. The 

question is why? 

51 
EXPLAINING HIGH BORDER PREFERENCE 

Let us consider some possible reasons why forest insects prefer forest borders. Forest border 

habitats are characterized by a great variety of 1) microsites and 2) tree and shrub species. For these 

reasons, rich insect species communities occur in these habitats. The existence of species variety is 

impossible within narrow local microclimatic conditions. However, since the forest borders are 

characterized by maximal amplitudes of microclimatic parameter fluctuations, they allow for the 

coexistence of insect species with different microclimatic requirements. 

It might be thought that all these factors relate only to phyllophages because xylophages depend 

on microclimatic conditions to a lesser degree and for them the availability of food is more important. 

Only the tree borders are subjected to strong winds and other unfavorable influences, however, and 

that circumstance makes for constant renewal of the food base by xylophagous insects. 

It is necessary, finally, to account for the preference of forest borders by cone and seed insects. 

Unlike the trees in forest thickets, border trees such as conifers may produce cones between "yield 

years." As a rule, only border and single-growing trees produce cones every year. Consequently, 

border habitats become refugia for cone and seed insects. This may also be a factor in the preference 

for forest borders by dendrophages. 

Thus we may conclude that: 1) forest borders and their analogues are preferable habitats for a 

great number of dendrophagous insects; 2) forest borders and their analogues are strategic sites for 

control of abundant forest insect species; and 3) forest borders may be used expressly for the analysis 

of fauna of dendrophagous species in certain forest ecosystems. 

52 
WOODY PLANT GRAZING SYSTEMS: 

NORTH AMERICAN OUTBREAK FOLIVORES 

AND THEIR HOST PLANTS 

WILLIAM J. MATISON\ DANIEL A. HERMS2

, 

JOHN A. WfiTER3, and DOUGLAS C. ALLEN4 

1USDA Forest Service 

North Central Forest Experiment Station 

1407 S. Harrison Road, East Lansing, MI 48823 U.S.A 

and 

Department of Entomology 

Pesticide Research Center, Michigan State University 

East Lansing, MI 48824 U.S.A 

2The Dow Gardens 

1018 W. Main St., Midland, MI 48640 U.S.A 

and 

Department of Entomology 

Pesticide Research Center, Michigan State University 

East Lansing, MI 48824 U.S.A 

3School of Natural Resources 

University of Michigan, Ann Arbor, MI 48104 U.S.A 

4College of Forestry and Environmental Sciences 

State University of New York 

Syracuse, New York 13210 U.S.A 

INTRODUCTION 

In North America, about 85 species of free feeding and leafmining folivorous insects in the 

orders Lepidoptera and Hymenoptera periodically cause serious and widespread defoliation of forest 

trees (Appendix 1 ). We call these insects expansive outbreak folivores based on the following criteria: 

1) population eruptions occur two or more times per 100 years, 2) severe host defoliation (> 50 

percent) occurs for 2 or more years per eruption, and 3) the area of each individual outbreak exceeds 

1,000 contiguous ha. There are about 20 other insects whose populations meet criteria one and two, 

but not criterion three. These we term local outbreak folivores and do not deal with them in this 

paper because they may operate on an entirely different scale than the expansive species. 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

53 
CHARACTERISTICS OF EXPANSIVE FOLIVORE OUTBREAKS 

Continent-Wide Infestation Area and Frequency 

Between 1957 and 1987 in the United States, at least 60 species caused outbreaks exceeding 

1,000 ha (USDA, Forest Service). The largest outbreak area (summed over many different geographic 

regions) caused by a single insect species (Malacosoma disstria) in a single year was 13.5 million ha 

(Appendix 2). At least 14 species had single-year infestation areas that covered 0.5 million ha. The 

four insects showing the most consistent outbreak frequency (> 25 yrs) as well as largest mean annual 

infestation areas ( > 0.5 million ha) were the eastern and western spruce budworms, Choristoneura 

fumiferana and C. occidentalis, respectively, the forest tent caterpillar, M. disstria, and the gypsy moth, 

Lymantria dispar (Table 1 ). These insects are largely in a league by themselves because most other 

species had less frequent and less expansive outbreak areas. Although we did not examine similar data 

from Canada, the pattern is likely to be much the same but with a bias toward folivores of Populus, 

Betula, and boreal conifers. For example, in 1975 C. fumiferana was at a century-high defoliation peak 

on more than 55 million ha in eastern Canada (Kettella 1983). On the average, at least 7.6 million ha 

were under severe defoliation each year by all species combined between 1957 and 1987 in the United 

States (Appendix 2). These are conservative estimates because of the difficulty of exactly delimiting the 

beginning, ending, and area of each outbreak. Generally, only the most severe cases are observed. 

Six Correlates of Defoliation Severity 

The impact of outbreak defoliations on forest stands differs with the insect species and the 

characteristics of the forest. Nevertheless, some generalities seem to hold regardless of the particulars 

of individual cases: 1) defoliation severity increases directly with homogeneity of the forest 

composition, 2) defoliation severity increases with the average amount of exposure of the individual 

tree crowns, 3) defoliation severity increases, though not necessarily linearly, with tree age, 

4) defoliation severity increases with warm, dry weather during the growing season, 5) defoliation 

severity increases with the folivore's predilection for polyphagy, and 6) the effects of defoliation on tree 

vigor are cumulative and not linear. These six factors may contribute to outbreaks for the following 

reasons: increasing the amount of available food per unit area (1,5) increases the insect's chances for 

survival and ultimate population growth; warmer, drier environments appear to favor folivorous insects 

(2,4) (Mattson and Haack 1987a, 1987b); and finally, as trees age, their crowns enlarge and they begin 

to flower, which can have both positive and negative effects on folivorous herbivores (see Herms and 

Mattson this volume). At the same time the trees become less suitable for sap feeders (Schowalter 

1989), which may have several important beneficial effects on free folivores (Mattson et al. 19S9). 

In North America, most cases of substantial tree mortality caused by outbreak folivores have 

occurred primarily in aging, "overmature" forests (Kinghorn 1954, Carroll 1956, McLeod 1970, Struble 

1972, Turnock 1972, Drooz 1980, Lynch and Witter 1984). However, site quality and tree vigor status 

interact significantly with tree age--low vigor trees growing on poor sites are much more vulnerable to 

death after outbreak folivory than are vigorous trees on rich sites (Mason and Tigner 1972, Turnock 

1972, Witter et al. 1975, Schultz and Allen 1977, Lynch and Witter 1984, Hix et al. 1987, Archambault 

et al. 1990). However, qualification is necessary here. Moderately poor sites may actually sustain less 

mortality per unit of defoliation than rich sites because the former tend to be under less intense plantplant competition and have trees with higher relative root and storage investments that allow them to 

tolerate both abiotic and biotic stresses. Rich sites induce more severe competition for space and light 

which favors individuals that invest proportionally more in canopy (Clark 1990). Accordingly, they 

have intrinsically higher rates of natural mortality owing to larger numbers of trees that are under 

severe competition and that invariably succumb during defoliation episodes (Clark 1990, Crow and 

Hicks 1990). 

54 
Table 1. Numbers of folivore species in different outbreak frequency classes, 

and mean annual area size classes between 1957 and 1987 in the 

United States. 

Mean annual outbreak area class: (1000 ha) 

Outbreak 

frequency 

class (yrs) 1-5 6-50 51-500 501-5000 

< 5 8 16 9 4 

< 10 0 9 4 2 

< 15 1 5 3 1 

< 20 0 0 3 0 

> 20 0 1 0 4 

Data derived from Appendix 2. 

High Grazing Tolerance: Woody Plant Grazing Systems 

We hypothesize that many natural plant systems that regularly support expansive outbreak 

folivores have only nominal regulatory (damage inducible) defenses against those folivores. The same 

is probably not true for other folivore guilds that are more truly parasitic, such as phloem and xylem 

sappers (Mattson et al. 1988b). And, it is certainly not the case for the inner-bark feeding guilds (see 

Mattson et al. 1988a ). In fact, the outbreak patterns observed for expansive folivores are an inevitable 

consequence of the plant's regulatory capacity. These plants have evolved only very weak capacities for 

regulating canopy herbivores because outbreak folivores generally have minimal impact on plant fitness. 

Note that this does not mean they have negligible impact on plant growth and reproduction. It means 

that when such impact occurs, it is nearly equally felt by all plants. For these reasons, we label them 

grazing systems as did McNaughton (1984, 1986) for certain grassland systems that are highly tolerant 

of and may be dependent on grazing by generalist mammalian herbivores. 

We do not imply that forest and grassland systems are identical, only that they are similar 

because folivory may be a fundamental part of the overall adaptive syndrome of both. Both systems, 

by virtue of their large areal sizes of relatively uniform plant form, are predisposed to chronic and 

substantial folivores--albeit of different types. Both also support folivores that exhibit substantial 

mobility and little host plant specificity (i.e. grazers, sensu McNaughton 1984, Thompson 1988). Their 

level of adaptation to and interaction with host plants is more at the scale of the landscape and biome 

rather than the individual plant. The physiological constraints and the ecological consequences that 

accompany a perennial, woody plant life history strategy cause the two kinds of systems to differ on the 

basis of their time scales. Woody plant grazing systems are defined by 1) their expansive, dense, and 

usually mono-oligodominant community structure that predisposes them to severe canopy herbivory, 

2) their capacity to physiologically tolerate consecutive seasons of high levels of grazing, 3) their 

capacity to ecologically tolerate grazing (maintain their competitive positions), 4) their generally low 

defenses against canopy herbivores, and 5) their commensalistic (indifference) or mutualistic dependence 

on folivory in fulfilling their life history strategy. That is, folivores have either a minor role or a very 

positive role in the plants' lif~ history (Mattson and Addy 1975). 

55 
CONDmONS SHAPING THE EVOLUTION OF PLANT DEFENSES 

Physiological Capacity to Recover From Folivory 

After experiencing herbivory, a plant must recover both physiologically and ecologically (Mattson 

et al. 1988b ). Both recovery processes influence the eventual evolution of plant defenses. In 

physiological recovery, herbivore removal of tissues or fluids, for which the plant has little or no 

capacity to replace or compensate for should elicit strong selection pressure for the evolution of 

powerful and fast acting defenses (McKey 1979, Rhoades 1979). For example, herbivore consumption 

of phloem/sapwood tissue is far more serious than equivalent biomass removal from the leaf canopy 

because the plant's capacity to compensate for the former is negligible compared to the latter. 

Moreover, damage to vascular tissues has strong, immediate negative repercussions to all other plant 

organs (canopy, roots, etc.), whereas damage to the canopy has less effect. Accordingly, the defensive 

systems of trees against inner-bark feeders are among the most powerful known in woody plants (see 

Mattson et al. 1988a ). 

On the other hand, leaves are one of the tissues that plants are most capable of replacing. 

However, the total physiological cost of losing and replacing leaves differs substantially with the size, 

resources, and adaptive strategy of the plant (Givnish 1988). Plants may compensate for low to 

moderate ( < 30 percent) levels of folivory by increased rates of photosynthesis in the other intact 

leaves due to 1) more light reaching lower and previously shaded leaves, 2) more water and nutrients 

available to the intact leaves, and 3) long-term acceleration of nutrient cycling (Mattson and Addy 

1975, Ericsson et al. 1980a, 1980b, McNaughton 1984, Verkaar 1988, Maschinski and Whitham 1989, 

Prins et al. 1989, Williamson et al. 1989). 

However, if folivory chronically exceeds a plant's capacity for tolerance, mortality can result 

directly from exhaustion of tree energy reserves or indirectly from secondary agents such as wood 

borers, bark beetles, and pathogens (Kinghorn 1954, Barbosa and Wagner 1989). 

Ecological Capacity to Recover: Plant-Plant Competition 

Although there is substantial evidence that severe defoliation can reduce tree growth and 

reproduction, and increase tree mortality, there is little substantive information about its impact on 

tree-tree competition. However, the important effects of folivory on non-woody plant competition and 

succession are much more widely appreciated (Cottam 1985, Cottam et al. 1986, Milchunas et al. 1988, 

Brown and Gange 1989, Crawley 1989a, 1989b, Jarosz et al. 1989, Polley and Detling 1989, Louda et 

al. 1990, Prins and Nell 1990a, 1990b ). Competition is pervasive in all plant communities; it is one of 

the principal ecological variables affecting the evolution of carbon allocation patterns. Thus, an 

understanding of the effects of herbivory on competition is crucial to interpreting its effects on the 

evolution of woody plant defenses (Taylor et al. 1990, Tilman 1990, Herms and Mattson 1991 ). 

CONDmONS FAVORING PLANT GROWTH INSTEAD OF DEFENSE 

In many systems prone to outbreaks, certain biological and ecological conditions interact to 

prevent the evolution of strong plant defenses against canopy folivory. For example, herbivory that 

occurs in overmature trees has little impact on fitness (except through effects on parent-progeny 

interactions) because such trees have already largely spent their reproductive capacity. 

56 
Oligospecies Plant Communities: Pioneer, Growth-Adapted Species 

Folivory occurring in vast, monodominant communities of rapidly growing species (such as those 

typically created when pioneering tree species invade en masse following extensive disturbances) has 

little chance of selecting for the evolution of powerful, regulatory plant defenses. First of all, the suite 

of plant traits that are conducive to successful competition in such environments is not physiologically 

compatible with high defensive investments (Huston and Smith 1987, Loehle 1988, Taylor et al. 1990, 

Tilman 1990). Fast growth is of paramount importance for competitive success, and defense will come 

at its expense (Harper 1989, Herms and Mattson 1991). This requires that plants maintain large foliar 

surface areas having high levels of leaf nutrients and water, and low levels of secondary metabolites 

(Gower and Richards 1990, Hilbert 1990). Such species have high capacity to outgrow others but low 

capacity to tolerate resource depletion (Tilman 1990), because competition for light is largely 

asymmetric (Wiener 1990). 

Second, in monodominated communities there is little evidence of consistent, long-term, 

differential herbivory among plants (although see Batzer 1969, Clancy this volume, Wagner this 

volume). Most outbreak folivores seem to exhibit little fine-tuned selectivity for individual host plants 

(Price et al. 1990). This is particularly true for macrolepidoptera on conifers, which seem to have 

broad host plant feeding capabilities (Holloway and Hebert 1979). Most often insect egg densities per 

tree increase directly with tree size or "target" area (Witter et al. 1975, Mattson et al. 1988c, Batzer et 

al. 1991) as would be expected if trees differ little in quality from the insect's perspective. 

Furthermore, larvae of these species exhibit little fidelity to their "mother" plant. In fact, in the case 

of Malacosoma disstria, the opposite is true: most larvae abandon their mother plant at about the 

third ins tar ~egardless of its current defoliation level (pers. observ. ). For many other species, larvae 

regularly disperse by ballooning when very small or by dropping and crawling when large (Coulson and 

Witter 1984, Barbosa et al. 1989)--dispersal mechanisms with very high risk of mortality and low 

probability of finely tuned host selection. 

Few studies have shown that inter-tree variation in folivory has a genetic basis (Mattson et al. 

1988b, Ayres et al. this volume), except where differences in tree phenology are the explanation (Witter 

and Waisanen 1978, Du Merle 1988). The scant existing evidence suggests that all members of the 

host population within a forest are nearly equally susceptible to defoliation, although this does not 

imply that all the trees are equally suitable for insect performance (Harris et al. 1982, Mattson et al. 

1988b, Schmid and Bennett 1988, Batzer et al. 1991 ). For example, during forest tent caterpillar 

outbreaks in trembling aspen forests (Populus tremuloides), virtually every member of the canopy 

community will be severely defoliated several times, including "nonhosts" that are never attacked when 

growing in isolation or in other communities. Defoliation also extends to most members of the small 

tree/shrub stratum, even into neighboring forest communities (Hodson 1941, Witter et al. 1975, pers. 

observ.). 

Uniform Folivory Favors Evolution of Tolerance 

Given that all members of the community receive equal levels of folivory during epidemics, can 

herbivory significantly alter the existing competition-derived fitness ranking of the member plants? We 

think not. Recovery is closely linked to size and growth capacity. Invariably, the suppressed, 

subdominant host trees quickly die, but they would probably not have survived thinning anyway. 

Severe defoliation shifts the competitive edge in favor of the larger and faster growing plants, selecting 

for tolerance traits, the capacity to quickly and strongly recover. We argue that tolerance capacity is 

the most likely evolutionary response by the plant population to folivory. Nonbiotic defoliation from 

hail, wind, and ice and snow storms may be more frequent (though not serially cumulative) than 

outbreak folivory and even more severe in some forests (Grier 1988), and it thus reinforces the 

evolution of general compensatory responses. 

57 
Physiological Cost of Leaves Increases with Plant Height 

If the physiological cost of leaves (sensu Givnish 1988) to such plants is low enough, they may 

be able to cope forever with severe herbivory through compensatory mechanisms, as some grasses do 

(McNaughton 1984, 1986). However, this is unlikely for taller, woody plants because the physiological 

cost of a leaf increases directly with its height above ground due to the added construction costs of 

stem and roots for support and nutrient transport (Givnish 1988). Hence, we speculate that there is a 

vertical size threshold, above which plants need to use some kind of low cost defenses for curtailing 

the long-term, severe herbivory that seems inevitable in vast monodominant communities. We and 

others hypothesize that these should build with canopy injury, i.e. delayed inducible resistance (DIR, 

sensu Haukioja and Neuvonen 1987, Bryant et al. 1988, Haukioja 1991) and should interfere minimally 

with plant growth and other recovery processes, but at the same time erode the herbivore's continued 

capacity to grow and multiply (Haukioja 1991 ). One extreme solution might be to produce no leaves 

for one generation of the folivore, thereby forcing its starvation. Although effective for strictly 

univoltine insects, it is not viable because the cost is too high, and bivoltinism and extended diapause 

are easy counteradaptions. A less extreme but nevertheless efficacious variation of this tactic, is to 

produce less nutritious leaves for the next several growing seasons that directly debilitate the herbivore 

and concomitantly cause it to be more susceptible to natural enemies (Myers 1988b, Edelstein-Keshet 

and Rausher 1989, Haukioja 1991 ). This is apparently the case for Betula resinifera and Populus 

tremuloides in Alaska (Werner 1979, 1981). Most DIR traits appear to be amplifications of existing 

constitutive secondary metabolite pathways (Tuomi et al. 1988a, 1988b, 1990), coupled to diminished 

nutrient levels. 

Can Natural Enemies Substitute for Delayed Inducible Resistance? 

The evolution of DIR will be favored to the extent that it contributes to outbreak decline 

before folivory precipitates widespread mortality due to exhaustion of plant reserves (and concomitant 

attack by wood borers) or competitive exclusion by some other nonhost species. At this point, cost of 

defense is no longer important because death is the alternative. However, if there are abundant, 

efficacious natural enemies (pathogens, parasitoids, predators) that are consistently capable of numerical 

responses to mounting folivore populations, then they may obviate the plant's need for DIR. Instead, 

the plants may need only to evolve strong recovery capacity and perhaps traits that enhance their 

natural enemies: nectar secretions, domatia (leaf structures which shelter predaceous mites), etc. 

(Mattson et al. 1989, Herms and Mattson 1991 ). 

Localized Rapid Inducible Resistance Complements Tolerance 

In resource-rich, oligo-dominant communities, highly sensitive, systemic, rapid inducible resistance 

(RIR ), and/or high levels of constitutive defenses are not viable tactics against free feeding folivores. 

Perpetual, whole-plant induction would chronically diminish the high growth rates that are fundamental 

to the basic life history strategy of such plants (Herms and Mattson 1991). However, very localized 

RIR may be a viable tactic if it serves only to disperse folivores among modules so as to reduce the 

average impact of folivory per plant (see Bogacheva this volume). In other words, RIR in this case 

functions primarily as a complement to physiologically based tolerance. However, RIR in these 

communities is not sufficient to prevent periodic, severe defoliation by "adapted" folivores because its 

proximate effects on behavior can be overwhelmed by starvation. Even biochemically very different, 

"nonhost" plants in and near the outbreak communities are stripped of their canopies. 

We propose, therefore, that selection pressure by herbivores favors primarily 1) high levels of 

tolerance to injury, coupled to 2) some form of low cost, highly localized RIR, and finally 3) densitydependent DIR that increases the probability of folivore mortality from natural enemies that build in 

response to herbivore populations. 

58 
Grow and Then Reproduce: an Evolutionarily Stable Strategy? 

Is it possible that herbivory in these communities could favor high levels of constitutive defenses, 

and/or a more powerful, regulatory defensive strategy? We think not. The underlying life history 

strategy of growth-dominated, shade-intolerant, pioneering plants provides strong physiological and 

ecological constraints to other evolutionary solutions (Huston and Smith 1987, van der Meijden et al. 

1988, Taylor et al. 1990). Competition for light by juvenile plants is so intense that rapid growth 

coupled to minimal defense systems will always be favored. For example, Makela (1985) concluded 

that the maximum fitness strategy in a dense, monodominant system will result from first growing as 

fast as possible and then switching to reproduction when the cost of further height growth is more 

than the cost of subsequent shading from neighbors. Because all individual plants often establish 

simultaneously and play by the same fundamental physiological rules, they end up highly synchronized 

throughout life and even in death (Mueller-Dombois 1987). Their simultaneous, wave-like or 

cohort-like decline may be a consequence of the entire adaptive syndrome. 

CONDffiONS FAVORING THE EVOLUTION OF STRONG DEFENSES 

Oligospecies Plant Communities: Stress Adapted Species 

Many of the preceding arguments apply also to oligospecies communities in low resource 

environments. However, the physiological capacity for tolerating and recovering from defoliation may 

now be substantially less than in high resource environments. This means that the physiological cost of 

leaf loss and replacement is much higher (sensu Givnish 1988). Hence, the adaptive strategy of 

stress-adapted plants requires a different mix of traits than those of growth-adapted plants (Huston and 

Smith 1987, Taylor et al. 1990). High rates of growth and leaf replacement are generally not 

sustainable due to shortages of critical resources (nutrients, water, etc). Therefore, plant emphasis is 

on the acquisition and efficient use of nutrients, low leaf turnover, and survival during critical drought 

and stress periods, etc. 

Thus, environmentally induced slow growth and longer leaf longevity (in evergreen species) 

create a high risk of injury from herbivores. At the same time, however, they significantly reduce the 

opportunity costs of defensive investments (Herms and Mattson 1991 ). Therefore, it should be 

adaptive that such plants should protect well their foliage, at least in direct proportion to each foliage 

cohort's contribution to plant vitality (McKey 1979, Rhoades 1979, Mattson et al. 1988b ). There is 

essentially a dichotomy between stress-adapted deciduous and evergreen species because of the different 

suites of adaptations that entail each kind of strategy (Bryant et al. 1988, Dickson 1989, 1991, Gower 

and Richards 1990). For example, the former tend to have higher rates of photosynthesis over a short 

photosynthetically active period and rely exclusively on storage for fueling each season's early growth. 

The latter have much lower rates of photosynthesis over a longer period and rely more on current 

photosynthates and leaf-stored nutrients to support early growth (Dickson 1989, 1991, Sprugel 1989). 

Foliage loss is more damaging to evergreen species because generally they do not refoliate in response 

to defoliation, and thus the losses must be integrated over the multi-year life span of such leaves. 

Uniform Herbivory Favors Tolerance 

A uniform plant community predisposes the plants to expansive outbreak herbivores and so does 

the wider tree spacing that often occurs on stressful sites. Under these circumstances, herbivore 

selection pressure still favors the evolution of tolerance to the degree that it is possible (in inverse 

relationship to the stress adaptation required). However, we hypothesize (Herms and Mattson 1991) 

that its complement, localized RIR, is not as adaptive in low as in high resource environments because 

of fundamental physiological and ecological constraints on its efficacious expression (especially in 

evergreen conifers). Furthermore, unlike the high resource case, folivory will favor additional, purely 

defensive traits that 1) reduce both the mean background level of herbivory and the likelihood of 

59 
herbivore population buildup, and 2) more swiftly stop herbivory once it has exceeded tolerance levels, 

i.e. a more powerful DIR. In the case of the first, higher levels of constitutive defenses and lower 

foliar nutritional quality will simultaneously reduce the overall herbivore species loading per plant (see 

Niemelii et al. 1982, Tahvanainen and Niemelii 1987) and lower the intrinsic rate of population 

increase of the many fewer adapted herbivore species. As for the second, there is good evidence in at 

least two deciduous tree-herbivore systems: Larix decidua/Zeiraphera dineana, and Betula pubescens 

tortuosa/Epirrita autumnata (Haukioja 1991 ). Likewise, the B. resinifera/Rheumaptera hastata and 

P. tremuloides/Choristoneura conjlictana systems in Alaska may qualify (Haukioja and Neuvonen 1987.) 

However, there is yet little substantive evidence for significant DIR in evergreen conifers (see 

Neuvonen and Niemelii in this volume). If DIR does occur, it is most likely to be manifested in 

currently produced foliage, which is probably the only leaf tissue physiologically capable of DIR 

(Leather et al. 1987, Wagner 1988, Buratti et al. 1990, Geri et al. 1990) and in fast growing seedlings 

and saplings (Karban 1990a, 1990b ). 

Small Size and Slow Growth Preclude Tolerance Responses 

Being very small predisposes young woody plants to the high probability of catastrophic, 

i.e. fatal, injury from herbivores merely because a small amount of herbivory is capable of devastating 

small plants. Normally, the risk of such injury would be small because it is spread widely among the 

vast number of individual seedlings that regenerate in cohort-like waves. However, slow growth 

compounds this risk significantly in direct relation to the time it takes to outgrow the risk of most 

such injury. Therefore small, slow growing, woody plants may die unless they use potent, deterrent 

constitutive defenses. 

Polyspecies Plant Communities: Pioneer, Growth-Adapted Species 

Selection pressure by herbivores for plant defenses is likely to be much more intense in 

polyspecies than in monospecies, pioneering communities. Consistent, differential herbivory among 

individual plants is more probable when the community is comprised of many species of plants. Each 

species, because of its inherent anatomicaVmorphological and biochemical uniqueness, tends to have its 

own suite of herbivores. Even polyphagous insects such as the gypsy moth show obvious host 

preferences. As a result, the preferred species are defoliated first and usually sustain the highest 

cumulative defoliation, and consequently, the highest mortality rates over an infestation episode (Crow 

and Hicks 1990). 

In brief, then, the selective pressure from folivores in a polyspecies, pioneering community is 

likely to be higher and different than in an oligospecies community. This should be expected because 

interspecies plant competition for light and nutrients will generally lead to different evolutionary 

adaptations than will primarily intraspecies competition (Aarssen 1989, Keddy and Shipley 1989, Barnes 

et al. 1990, Connolly et al. 1990). 

However, the high growth strategy of such plants entails a suite of correlated physiological and 

ecological traits that may constrain costly defensive investments. Therefore, we hypothesize that 

different, but ecologically equivalent, defensive tactics will evolve as a result of plants balancing 

investments in defenses against growth (including reproduction). The diversity of evolutionary solutions 

will depend on the number of competing plant species. One solution might be high growth and low 

constitutive defenses with concomitantly higher species loading per plant, while another might be 

medium growth with higher standing defense and lower herbivory per plant, and so on. For example, 

Prins and Neils (1990a, 1990b) and Prins et al. (1989) have elegantly shown that two competing 

herbaceous plant species can experience vastly different levels of herbivory, and can coexist because of 

different leaf tissue chemistries and specific elements of their life history strategies. 

60 
Defenses Vary in Relation to Intensity of Plant Competition 

The strength of the DIR defensive response will vary with the time scale of plant-plant 

competition. Where interspecific competition is intense (e.g. rich sites) and debilitation over successive 

growing seasons can cause a serious loss in competitive status, we predict powerful, fast acting defenses 

that will impact the next generation of the herbivore. At the other end of the continuum, where 

competition is less intense and debilitation over two growing seasons does not seriously jeopardize an 

individual's competitive status, then "slower" defenses (within two to three growing seasons) are 

adequate. 

Because competition is not constant over the course of plant ontogeny, constitutive and 

inducible defenses may also vary with the plant ontogeny in direct relation to competition. For 

example, per capita mortality rate curves for trees often are believed to be U-shaped, i.e. high mortality 

due to density independent factors and competition (other trees, shrubs, herbaceous matter, etc.) during 

the early period of establishment, followed by lower and relatively stable tree-tree competition-induced 

mortality up to old age, when mortality rates may rise again due to senescence (Harcombe 1987, Clark 

1990). Hence, herbivore injury may be more critical in early life when plants are also more susceptible 

to competitive displacement. At this time, therefore, defenses would be desirable to prevent the 

compounding negative effects of herbivory. However, they should not come at the expense of 

competitive capacity (i.e. growth). One solution is escape as implied by Janzen (1970), who predicted 

that the success of such understory propagules will increase with their distance from parents or like 

conspecifics. Apparently, this is being borne out in tropical forests (Clark 1986). Other solutions 

would be low cost defenses such as bioassociations, or low concentrations of highly toxic, deterrent 

secondary ch~micals (Herms and Mattson 1991 ). 

Polyspecies Community: Shade-Tolerant Species 

Shade tolerant species in polyspecies communities clearly require stronger defenses. Their 

strategy, at least in their early years, is often one of competition tolerance, the capacity to endure, to 

subsist on the meager amounts of light that reach the dimly lit forest understory (Givnish 1988, Taylor 

et al. 1990). One would expect, based on their unique suite of physiological and ecological traits, that 

they should also differ markedly from pioneering species in their evolutionary responses to herbivory 

(Loehle 1988, Taylor et al. 1990). Long periods of slow growth in low light (light stress) require 

strong defenses to survive prolonged exposure to mammalian and micro-herbivores. Because plant 

recovery capacity will be very limited, strong, highly effective constitutive defenses that drastically lower 

the herbivore loading per plant should be highly adaptive. 

The capacity of such plants to tolerate herbivory may be so limited that neither localized RIR 

nor general DIR is a viable evolutionary option for understory plants, at least not until those plants 

are released from shade stress and growing substantially above their whole-plant, physiological 

compensation point (Givnish 1988). In fact, when occupying full light (e.g. full canopy position), they 

may exhibit some of the characteristics of pioneering species. In other words, some plants may have 

two suites of adaptive syndromes: one when subjected to very low light and the other when subjected 

to medium-full light and capable of faster growth. Such is apparently the case for sugar maple, Acer 

saccharum, a very shade tolerant tree species in eastern North America (Canham 1989). 

Polyspecies Plant Communities: Conversion To Monodominance 

Some polyspecies communities can eventually become oligospecies, monodominated communities 

(if left undisturbed) because of steadily increasing recruitment by species that have the least demand 

for light. This commonly happens in the Great Lakes Region where sugar maple and balsam fir often 

assume complete dominance in their respective mixed species forests (in the absence of fire) because of 

their superior shade tolerance and highly aggressive recruitment under their own canopies (Bourdo 

61 
1969, Tubbs 1969). This is also a well-established phenomenon in the world's tropical forests (Hart et 

al. 1989). Such single-species dominated, late successional forests can eventually become extensive over 

time. Hence, like the oligospecies, pioneer tree species forests, they may be highly prone to outbreak 

folivores. However, unlike the pioneer species, the late successional species have evolved in an 

environmental matrix consisting of polyspecies competition and shade tolerance. Some of the 

physiological traits needed for success there will likely carry over into those environments where the 

forest acquires monospecific dominance: stronger constitutive defenses, weaker DIR, lower tolerance 

capacity. On the other hand, such a plant species may be phenotypically plastic so that it acquires 

some of the traits of a pioneering tree species when growing monodominantly in full sunlight. 

CHARACTERISTICS OF OUTBREAK FOREST SYSTEMS 

Oligospecies Forests: Extremes of Shade Tolerance 

There are about 85 species of expansive outbreak folivores in North America, but the number of 

plant systems supporting these insects is substantially smaller, between 30 and 40. Thus, some plant 

systems support more than one outbreak species: e.g. A. balsamea/Picea spp.: 4, A. saccharum/Fagus 

grandifolia: 5, Pinus contorta: 1, P. tremu/oides: 8, Pseudostuga menziesii: 8, etc. (Appendix 3). 

Likewise, some insect species have several races that can reach outbreak proportions in more 

than one system: e.g. Malacosoma disstria in A. saccharum, N. sylvatica, P. tremuloides, and Quercus 

spp. forests. 

Almost all these outbreak systems are oligospecies communities dominated by just one or two 

plant species (e.g. P. tremuloides, Betula papyrifera, A. saccharum/F. grandifolia, Pinus banksiana, Pinus 

ponderosa, A. balsamea, etc.). These species tend to fall largely into either one of two shade tolerance 

classifications: 1) highly light demanding, i.e. shade intolerant, or 2) highly shade tolerant, and capable 

of developing into monodominant communities (Appendix 3). This classification may also apply to 

outbreak forest systems in the tropics (Bruenig and Huang 1989). Some oak species exhibit medium 

shade tolerance and thus may be an exception. 

Predictions of Insect Loading, Outbreak Frequency, Duration 

The following predictions can be derived from the preceding discussions of plant life history 

strategies: 

1) folivores species loading, and mean level of herbivory should rank as follows: pioneering, 

growth-adapted species (PGAS) > pioneering, stress-adapted, deciduous species (PSASd) > 

pioneering, stress-adapted, evergreen species (PSASe) > competition- and shade-tolerance 

adapted species (CSTS); 

2) the frequency of outbreaks per unit life span should rank as follows: PGAS > PSASd > 

PSASe > CSTS; 

3) the duration of outbreaks should rank as follows: PSASe > PGAS > PSASd > CSAS. 

This ranking reflects the limited capacity of some stress-adapted plants, especially evergreen conifers, to 

exhibit substantive, efficacious inducible defenses of any kind (RIR, DIR) (Bryant et al. 1988, 

Neuvonen and NiemeUi this volume, Herms and Mattson 1991 ). For example, severe defoliation of 

evergreen conifers can lead to an increase in adventitious sprouting and a general increase in foliar 

nitrogen (Batzer 1969, Goyer et al. 1990, I..AngstrOm et al. 1990, Piene and Little 1990). The net 

result may ameliorate rather than deteriorate foliage quality for herbivores (Haukioja 1991, Haukioja et 

62 
al. 1990) at least until substantial rootlet mortality causes nutrient impoverishment to be more severe 

than plant carbon limitations. 

Outbreak Patterns by Plant Growth and Shade Tolerance Classes 

Outbreak Frequency 

There is very little information regarding the number of outbreaks that occur during the life 

span of a given tree species under given site conditions. Instead, most information concerns insect 

dynamics over broad geographic regions (Myers 1988a). Thus, it is difficult to generate sound 

generalizations about differences in outbreak patterns among tree species. For most short-lived species 

( < 125 yrs), the data suggest that at least two outbreak episodes occur, invariably during the second 

half of the life span of these species. For some longer lived species, such as P. menzeisii, several 

outbreak episodes are likely during the second half of their life span (Swetnam and Lynch 1989). For 

other species, however, there is not enough information to make any conclusions. 

In a few cases, obvious, regular patterns have been recognized in middle-aged to older trees: 

the apparent 5-year and 10- to 15-year-cycles of M. disstria on Nyssa aquatica (Goyer et al. 1990), and 

P. tremuloides, respectively (Hodson 1941, pers. observ.), the 10- to 15-year-cycles of Acleris variana 

(Miller 1966), the 35-40 year cycles of C. fumiferana on A. balsamea (Royama 1984), and the apparent 

10-year-cycles of Orgyia pseudostugata and 28-year-cycles of C. occidentalis on P. menzeisii in British 

Colombia (Myers 1988a, Shepherd et al. 1988). 

Outbreak Duration 

Only slightly more information is available about the average duration of outbreaks (Table 2). 

To look for trends in duration of defoliation by plant life history strategies, we classified insects on the 

basis of the shade tolerance and the growth rates of their primary host trees (Table 3). Few obvious 

patterns emerged. This is not altogether surprising, given the vagueness of the available data. 

Typically, most outbreaks lasted 2 to 3 years, regardless of the host plant's growth/shade classification 

(Tables 2, 3). However, some unusually chronic cases are associated with conifers and/or leaf miners: 

Coleotechnites spp. on Pinus contorta (> 10 yrs), Pristiphora erichsonii on Larix laricina (> 6 yrs), 

Choristoneura spp. on Abies spp. and P. menzeisii (> 6 yrs), Archips argyrospila on Taxodium distichum 

(> 5 yrs), and the maple leaf cutter, Paraclemensia acerifoliella, on Acer saccharum (> 4 yrs) (Ross 

1962, Struble 1972, Turnock 1972, Swetnam and Lynch 1989, Goyer et al. 1990, see also Neuvonen and 

Niemela in this volume). 

Effects of Natural Enemies on Outbreak Patterns 

Because host effects on folivore population dynamics are naturally confounded with natural 

enemy effects, it is difficult to tease apart the two (McNamee et al. 1981, Hanski 1987, Goyer et al. 

1990). For example, it seems that most outbreak folivores are prone to bacterial, fungal, and viral 

epizootics that may limit their population outbreaks to about 3 years (Myers 1988a, Shepherd et al. 

1988). If it is generally the case that natural enemies limit the duration of outbreaks, then one may 

have to seek enemy-free conditions to test the true host effects on folivore dynamics. For example, 

Shepherd et al. (1988) reported that where virus was not evident in 0. pseudotsugata outbreaks, they 

either ended quickly by killing the host plants or they lasted for as long as 9-12 years on isolated 

Picea spp. Goyer et al. (1990) concluded that in permanently flooded T. distichum and N. aquatica 

wetlands where parasites and predators of folivores are scarce, A. argyrospila and M. disstria populations 

cycle continuously in response to foliage depletion. Other authors have also concluded that natural 

enemy-impoverished habitats are prone to more frequent and severe outbreaks of folivores (Tumock 

1972, Hanski 1987, Mason 1987). 

63 
Table 2. Average duration (years) of outbreaks by different insects in North 

America. 

Species Years Species Years 

Acleris gloverana 2-3 Heterocampa manteo 2 

Acleris variana 2 Lambdina fiscellaria lugubrosa 3 

Arch ips argyrospila 5 Malacosoma americanum 2-3 

Archips semiferanus 2 Malacosoma disstria1 3 

Bucculatrix candensisella 2-3 Malacosoma californicum 3-5 

Choristoneura conflictana 2-3 Melanolophia imitata 2 

Choristoneura fumiferana 5-8 Neodiprion pratti banksianae 2-3 

Choristoneura occidental is 3-6 Neodiprion swainei 3-4 

Choristoneura pinus 2-4 Nymphalis californicum 1-2 

Coleotechnites milleri 10-20 Orgyia pseudotsugata 1-3 

Coleotechnites starki 10-20 Paraclemensia acerifoliella 3-6 

Coloradia pandora 6-8 Parorgyia grisefacta 3 

Datana integerrima 2 Pristiphora erichsonii 3-20 

Dryocampa rubicunda 2 Rheumaptera hastata 2 

Hetercampa guttivita 1-3 

Table 3. Comparing the duration of insect outbreaks by tree growth rates and 

shade tolerance classifications. Each number in the table 

represents an average outbreak period in years for an insect species 

that occurs on a host having that growth and shade classification. 

Growth Low shade Medium shade High shade 

rate2 tolerance2 tolerance tolerance 

Low 2,3,7,15,15 2,5 2,2,2,4 

Medium 2,3,3 2 3,3,3 

High 2,2,2,3,3,3,3,3,4,6 n.a. 2,6 

Very high 3,3,3 n.a. n.a. 

1M. disstria in aspen forests. 

2Data about tree classes derived from Appendix 3. 

64 
CLASSIFYING GRAZING SYSTEMS IN NORTH AMERICA 

Although there may be only 85 species of outbreak folivores in North America, they annually 

chew their way though about 7.6 million ha of tree leaves across the United States (USDA, Forest 

Service). Most of the forests impacted by outbreaks support more than one species of outbreak 

folivore and sustain at least two severe defoliation episodes. Yet the forests survive, even though in 

some unique cases most overs tory individuals die as a result of the defoliations (e.g. Choristoneura spp. 

on Abies spp. ). Most vigorous trees, in fact, have the capacity to physiologically tolerate 2 successive 

years of near complete defoliation of current-year foliage. Moreover, those trees that grow in vast 

monodominant stands are not subject to the usual interspecies competitive encroachment that occurs 

during such outbreaks. The following is a partial description of three different types of grazing 

systems: chronic, coup-de-grace, and limited systems. 

Chronic Grazing Systems: Short-lived, Growth-Adapted Pioneers 

In the case of most folivores that do not usually cause tree mortality, we argue that folivory is 

not so much a mutualistic as it is a commensalistic consequence of the plant's "life-style." Outbreak 

folivores are inevitable where plants grow in vast, monodominant, largely even-aged, pioneer 

communities. We label those as "chronic grazing systems," which by virtue of their short lifespan, high 

growth strategy, and low competition tolerance, cannot make substantive investments in defense. 

Chronic herbivory can be physiologically tolerated with little or no consequence to the competitive 

status of individuals--barring compounding stresses such as severe moisture deficits or excesses, and 

pollution. Such systems would be those dominated by P. tremuloides, B. papyrifera, N. aquatica, and 

perhaps some intolerant, fast-growing conifers such as P. banksiana, interior P. menzeisii, and 

L. laricina. 

Coup-de-Grace Grazing Systems: Short-lived, Shade-Tolerant Species--Abies spp. 

True firs and tortricids appear to be a special case, i.e. a "coup-de-grace grazing system." For 

example, the interaction between C. fumiferana and A. balsamea/Picea spp. forests in eastern North 

America may be highly coevolved because it apparently dates back at least 8,000-10,000 years 

(Anderson et al. 1986). Clearly, A. balsamea is not threatened by its association with C. fumiferana 

even though substantial mortality invariably results when outbreaks occur in mature stands (MacLean 

1980). Such mortality increases nonlinearly with the age of the stand, the percentage basal area in 

balsam and spruce, and the severity of moisture stress (Batzer 1969, MacLean 1980, Hardy et al. 1983, 

Lynch and Witter 1984, Archambault et al. 1990). In fact, it is likely that the insect enhances balsam's 

ability to compete with other trees. Being shorter lived, faster growing, and more shade tolerant than 

its common associates (P. glauca, P. rubens, P. mariana), balsam competes by more rapidly turning over 

its populations, aided by wind, root, and stem herbivores, and C. fumiferana (Sprugel and Bormann 

1981, Harcombe 1987, l..oehle 1988). The spruces, on the other hand, are much less subject to windthrow and defoliation-induced mortality (Archambault et al. 1990, MacLean 1980) and compete through 

their greater persistence (Gordon 1985). However, attaining larger size and older age is not always 

adaptive where the growing season is cold limited and where soils are shallow and nutrient poor. 

Givnish (1988) argued that because foliage costs increase substantially with tree height, the whole plant 

ecological compensation point dictates a smaller stature in resource limited environments. 

Limited Grazing Systems: Long-lived, Shade- and Stress-tolerant Species 

Shade-adapted species such as A. saccharum/F. grandifolia, and Tsuga spp., as well as the longlived, stress-adapted species such as some Quercus spp., and Pinus spp. (e.g. P. ponderosa) may have 

very limited physiological capacity to tolerate severe, prolonged defoliation, especially as they reach 

65 
maturity. Hence, we classify systems dominated by these as "limited grazing systems." They are subject 

to extinction unless defoliation is in some sense limited, either quantitatively or qualitatively. 

For example, the evergreen conifers may be able to cope much longer, if new growth is spared 

and folivory is strictly confined to older age classes of needles as is the case for sawflies (Diprionidae) 

and some lepidopterans such as the pandora moth, Coloradia pandora. 

SUMMARY 

High growth-adapted, short-lived plant species that form mono- and oligo-dominated systems are 

most susceptible to and most capable of tolerating chronic defoliation (Table 4). These plants tend to 

be shade intolerant and invest a very large fraction of their resources into enlargement of their 

canopies which have high nutrient and low allelochemical levels, i.e. high specific leaf areas. 

High stress-adapted species that form mono- and oligo-dominant systems are also very 

susceptible to but not highly tolerant of chronic, severe defoliation (Table 4). Consequently they ought 

to have evolved defensive mechanisms to limit the frequency, duration, and the nature of folivory. 

They will have high levels of foliar allelochemicals, low levels of nutrients, and perhaps a significant 

delayed inducible defense--at least for deciduous species. 

Table 4. Defensive responses3 evolved against folivores by plants that have 

different life history strategies. 

High growth 

adapted 

High stress 

adapted 

Monodominant-adapted 

life history 

Deciduous 

Tol. high 

Con. low 

RIR weak 

DIR weak 

Tol. low 

Con. high 

RIR weak 

DIR med. 

Evergreen 

Tol. med.4 

Con. med. 

RIR weak 

DIR weak 

Tol. low 

Con. v. high 

RIR none 

DIR none 

Polydominant-adapted 

life history 

Deciduous 

Tol. med. 

Con. med. 

RIR strong 

DIR strong 

Tol. v. low 

Con. v. high 

RIR weak 

DIR med. 

Evergreen 

Tol. low 

Con. high 

RIR med. 

DIR med. 

Tol. v. low 

Con. v. high 

RIR none 

DIR none 

3Tol. - tolerance capacity, Con. - constitutive defense level, RIR and 

DIR - rapid inducible and delayed inducible resistance, respectively. 

4Med ... medium 

66 
Growth-adapted, short-lived, shade tolerant plant species that form polydominant plant systems 

when young, but monodominant when older, may have the phenotypic plasticity to exhibit a blend of 

strategies for coping with outbreak folivores. When slow growing in heavy light competition with other 

species, they may be highly defended against folivores. On the other hand, when older and growing 

monodominantly they may rely more on tolerance and defenses similar to those of the shade intolerant 

group. 

ACKNOWLEDGEMENTS 

This manuscript was largely developed while the senior author (WJM) was on sabbatical leave at 

the INRA Station de Zoologie Forestiere in Ardon-45160 Olivet, France. Dr. Jean Levieux and 

numerous staff there deserve special thanks for providing the necessary intellectual atmosphere and 

support that allowed the fruition of this work. The authors also gratefully acknowledge the 

contributions emanating from their challenging discussions with Dr. P. NiemeUi, Dr. E. Haukioja, 

Mr. M. Ayres, and Dr. S. Larsson. They also thank Dr. B. Wickman, Dr. M. Wagner, Dr. R. Mason, 

and Dr. P. Rush for sharing their observations, unpublished data, and research documents. 

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74 
APPENDIX 1 

Outbreak folivores in North America and their primary host plants. 

Genus Species Family Primary host plant 

Acleris glover ana Tortricidae Tsuga heterophylla 

variana Tortricidae Abies balsamea 

Alsophila pometaria Geometridae Quercus spp. 

Anacamptodes ephyraria Geometridae Taxodium distichum 

Anisota senator is Saturniidae Quercus spp. 

Arch ips argyrospilus Tortricidae Quercus spp. 

argyrospilus Taxodium distichum 

semiferanus Quercus ellipsoidalis 

Argyresthia thuiella Argyresthiidae Thuja occidentalis 

Argyrotaenia tubulana Tortricidae Pinus contorts 

Bucculatrix canadensisella Lyonetiidae Betula papyrifera 

Caliroa spp. Tenthredinidae Quercus spp. 

Choristoneura biennis Tortricidae Abies lasiocarpa 

conflictana Populus tremuloides 

fumiferana Abies balsamea 

lambertiana Pinus contorts 

occidental is Pseudotsuga menziesii 

orae Abies amabalis 

pinus Pinus banksiana 

retiniana Abies concolor 

viridis Abies concolor 

Coleophora laricella Coleophoridae Larix laricina 

serratella Betula papyrifera 

Coleotechnites milleri Gelechiiidae Pinus contorts 

starki Pinus contorts 

Coloradia pandora Sphingidae Pinus contort a 

pandora Pinus jeffreyii 

pandora Pinus ponderosa 

Dasychira pinicola Lymantriidae Pinus banksiana 

Datana integerrima Notodontidae Cary a illinoensis 

Diapheromera femorata Phasmatidae Quercus rubra 

Diprion simi lis Diprionidae Pinus strobus 

Dryocampa rubicunda Saturniidae Acer spp. 

Ectropis crepuscular is Geometridae Tsuga heterophylla 

Ennomos subsignarius Geometridae Carya spp. 

Epinotia meritana Olethreutidae Abies concolor 

solandriana Betula papyrifera 

tsugana Tsuga heterophylla 

Epirrita autumnata omissa Geometridae Tsuga heterophylla 

Erannis tiliaria Geometridae Acer saccharum 

Fenusa pusilla Tenthredinidae Betula papyrifera 

Galenaria consimilis Geometridae Pseudotsuga menziesii 

Halisidota argentata Arctiidae Tsuga heterophylla 

75 
APPENDIX 1 continued 

Genus Species Family Primary host plant 

argentata subalpina Juniperus scopulorum 

Heterocampa guttivita Notodontidae Fagus grandifolia 

manteo Quercus alba 

Hydria prunivorata Geometridae Prunus serotina 

Gracillariidae Populus tremuloides 

Lithocolettis ontario 

Lamb dina fiscellaria fiscellari Geometridae 

fiscellaria lugubrosa Tsuga heterophylla 

fiscellaria somniaria Quercus garryana 

punctata Quercus gambelii 

Lyman tria dis par Lymantriidae Quercus spp. 

Malacosoma americanum Lasiocampidae Prunus serotina 

californicum fragile Lasiocampidae Populus tremuloides 

constrictum Quercus douglasii 

disstria Acer saccharum 

dis stria Nyssa aquatics 

disstria Populus tremuloides 

dis stria Quercus spp. 

Melanolophia imitata Geometridae Pseudotsuga menziesii 

Neodiprion abietis Diprionidae Abies balsamea 

abietis Abies concolor 

burkei Pinus contorts 

educolis Pinus edulis 

excitans Pinus taedae 

gillettei Pinus ponderosa 

lecontei Pinus resinosa 

nanulus contortae Pinus contorts 

pratti banksianae Pinus banksiana 

pratti pratti Pinus virginiana 

swainei Pinus banksiana 

taedae linearis Pinus taedae 

tsugae Tsuga heterophylla 

Neophasia menapia Pieridae Pinus ponderosa 

Nepytia freemani Geometridae Pseudotsuga menziesii 

phantasmaria Pseudotsuga menziesii 

Odontota dorsalis Chrysomelidae Robinia pseudoacacia 

Operophtera bruceata Geometridae Acer saccharum 

bruceata Populus tremuloides 

Orgyia pseudotsugata Lymantriidae Abies grandis 

pseudotsugata Pseudotsuga menziesii 

Paraclemensia acerifoliella Incurvariidae Acer saccharum 

Parorgyia grisefacta Lymantriidae Pinus ponderosa 

Phaeoura mexicanaria Geometridae Pinus ponderosa 

Phryganidia californica Dioptidae Quercus lobata 

Phyllocnistis populiella Gracillariidae Populus tremuloides 

76 
APPENDIX 1 continued 

Genus 

Pristiphora 

Rheumaptera 

Sciaphila 

Semiothisa 

Symmerista 

Xylomgyges 

Zeiraphera 

Zelleria 

Species 

erichsonii 

hastata 

simplex 

sexmaculata 

albifrons 

canicosta 

simplex 

hesperiana 

improbana 

haimbachi 

Family 

Tenthredinidae 

Geometridae 

Olethreutidae 

Geometridae 

Notodontidae 

Noctuidae 

Olethreutidae 

Yponomeutidae 

Primary host plant 

Larix laricina 

Betula papyrifera 

Populus tremuloides 

Larix laricina 

Acer saccharum 

Quercus alba 

Pseudotsuga menziesii 

Pseudotsuga menziesii 

Larix occidentalis 

Pinus ponderosa 

Data derived from Furniss and Carolin 1977, Drooz 1985, and others. 

77 
APPENDIX 2 

Size (ha) and frequency of outbreak areas by different folivore species in the 

United States during a 28-year period between 1957 and 1987. Derived from 

Annual Pest Reports by USDA, Forest Service. 

Average5 Maximum Frequency Average6 

Outbreak insect species area/episode area (yrs) area/year 

Acanthodyla circumcinta 36,437 36,437 1 1,301 

Acleris gloverana 3,980 27,530 12 1,706 

Acleris variana 39,472 115,789 5 7,049 

Alsophila pometaria 82,195 450,607 16 46,969 

Anacamptodes vellivolata 20,243 20,243 1 723 

Anisota sanatoria 1,113 2,105 2 80 

Archips argyrospila 19,555 47,773 10 6,984 

Archips semiferanus 420,520 1,417,004 6 90,111 

Argyresthia thuiella 52,632 52,632 1 1,880 

Bucculatrix candensisella 6,073 8,097 2 434 

Argyrotaenia gogana 41,970 80,972 3 4,497 

Caliroa spp. 735,830 1,336,032 2 52,559 

Choristoneura cam ana 39,541 52,632 3 4,237 

Choristoneura conflictana 362,295 2,631,579 19 245,843 

Choristoneura fumiferana 1,384,858 3,103,644 26 1,285,940 

Choristoneura lambertiana 26,846 109,717 8 7,670 

Choristoneura occidental is 2,290,445 5,353,610 28 2,290,445 

Choristoneura orae 1,923 2,713 2 137 

Choristoneura pinus 99,154 379,352 16 56,659 

Choristoneura retiniana 152,591 224,049 4 21,799 

Choristoneura viridis 43,015 143,320 5 7,681 

Coleophora laricella 1,183,240 12,064,777 12 507,103 

Coleotechnites milleri 105,457 242,915 13 48,962 

Coloradia pandora 6,904 18,016 13 3,205 

Croesia albicomana 140,663 323,887 4 20,095 

Daschyra pinicola 7,535 25,709 9 2,422 

Diaphemorata femorata 19,703 54,656 6 4,222 

Diprion similis 974,176 1,943,320 2 69,584 

Dryocampa rubicunda 12,551 24,291 2 896 

Ennomos subsignarius 300,174 620,243 7 75,043 

Epinotia meritana 8,967 47,368 11 3,523 

Epinotia solandriana 14,650 59,166 6 3,139 

Erannis tiliaria 1,754 4,049 3 188 

Galenaria consimilis 1,518 2,429 2 108 

5Infestation areas summed over the entire United States and divided by 

frequency (yrs). 

6Average area x frequency+ 28. 

78 
APPENDIX 2 continued 

Outbreak insect species 

Average 

area/episode 

Halisodota argentata alpina 2,699 

Heterocampa guttivita 125,586 

Heterocampa manteo 544,356 

Hydria prunivorata 85,425 

Ichthyura inclusa 6,680 

Lambdina anthasaria 17,304 

Lambdina fiscellaria fiscellar 207 

Lambdin a fiscellaria somniaria 826 

Lamb dina fiscellaria lugubrosa 8,085 

Lithocolletis ontario 109,603 

Lithophane antennata 42,510 

Lymantria dispar 774,275 

Malacosoma disstria 934,676 

Malcosoma californicum fragile 30,476 

Nacophora mexicanara 3,684 

Neodiprion pratti paradoxicus 422,348 

Neodiprion abietis 7,547 

Neodiprion educolis 101,215 

Neodiprion excitans 22,901 

Neodiprion gillettii 810 

Neodiprion lecontei 908 

Neodiprion nanulus contortae 2,834 

Neodiprion pratti banksianae 24,291 

Neodiprion pratti pratti 633,907 

Neodiprion taeda linearis 45,443 

Neodiprion tsugae 11,985 

Neophasia menapia 9,075 

Neptyia freemani 904 

Opheropthera bruceata 60,134 

Orgyia pseudotsugata 36,433 

Paleacrita vernata 5,465,775 

Paraclemensia acerifoliella 9,399 

Phyllocnistis populiella 202,429 

Pristiphora erichsonii 85,701 

Rheumaptera hastata 485,946 

Sciphila duplex 37,454 

Semiothisa sexmaculata 101,822 

Stilpnotia salicis 3,644 

Symmerista albicosta 13,360 

Symmerista canicosta 220,951 

Xylomyges simplex 3,239 

Zeiraphera griseana 81,344 

Zeiraphera hesperiana 45,142 

79 

Maximum 

·area 

4,049 

465,587 

2,226,721 

163,968 

6,680 

17,304 

405 

842 

28,340 

209,085 

80,972 

5,263,158 

13,461,538 

121,943 

6,073 

422,348 

16,194 

101,215 

121,457 

810 

2,632 

3,239 

36,437 

1,113,360 

275,992 

28,664 

30,769 

1,417 

152,227 

323,887 

10,931,174 

24,291 

202,429 

202,429 

2,359,919 

68,826 

202,429 

3,644 

18,219 

526,316 

3,239 

209,717 

49,798 

Frequency 

(yrs) 

3 

14 

6 

6 

1 

1 

2 

2 

8 

2 

2 

26 

28 

16 

2 

1 

3 

3 

6 

1 

6 

2 

2 

4 

9 

8 

8 

3 

5 

21 

2 

3 

3 

11 

9 

4 

2 

1 

2 

4 

1 

6 

2 

Average 

areajyear 

289 

62,793 

116,648 

18,305 

239 

618 

15 

59 

2,310 

7,829 

3,036 

718,970 

934,676 

17,415 

263 

15,084 

809 

10,844 

4,907 

29 

195 

202 

1,735 

90,558 

14,607 

3,424 

2,593 

97 

10,738 

27,325 

390,413 

1,007 

21,689 

33,668 

156,197 

5,351 

7,273 

130 

954 

31,564 

116 

17,431 

3,224 
APPENDIX 2 continued 

Outbreak insect species 

Zeiraphera improbana 

Zeiraphera ratzeburgiana 

Zelleria haimbachi 

Grand total area/year 

Average 

area/episode 

17,465 

34,818 

15,083 

80 

Maximum 

area 

61,134 

34,818 

69,636 

Frequency 

(yrs) 

4 

1 

11 

Average 

area/year 

2,495 

1,243 

5,926 

7,618,488 
APPENDIX 3 

Outbreak host plant systems and their outbreak folivores in North America defined b) 

the dominant plant species. Shade tolerance and growth rate classifications, 7 

typical age of mortality from Loehle (1988), and percent host domination of system 

from various sources, primarily Folwells (1965). 

Host plant parameters 

Average Percent 

Shade Growth age at system Outbreak 

Species tolerance rate death domination folivore species 

Abies amabalis 4 3 400 so Choristoneura orae 

Abies balsamea 5 4 125 so Acleris variana 

Choristoneura fumiferana 

Lambdina fiscellaria fiscella 

Neodiprion abietis 

Abies concolor 5 3 10 50 Choristoneura retiniana 

Choristoneura viridis 

Epinotia meritana 

Neodiprion abietis 

Abies grand is 4 3 200 60 Orgyia pseudotsugata 

Abies lasiocarpa 5 3 150 65 Choristoneura biennis 

Acer saccharum 5 2 300 so Erannis tiliaria 

Malacosoma disstria 

Operophtera bruceata 

Paraclemensia acerifoliella 

Symmerista albifrons 

Acer rubrum 5 2 150 so Dryocampa rubicunda 

Betula papyrifera 2 4 100 75 Bucculatrix canadensisella 

Coleophora serratella 

Epinotia solandriana 

Fenusa pusilla 

Rheumaptera hastata 

Cary a illinoensis 2 3 300 50 Datana integerrima 

Cary a spp. 2 2 200 n.a. Ennomos subsignarius 

7classes range from 1 to 5, low to high, respectively. 

81 
APPENDIX 3 continued 

Host plant parameters 

Average 

Shade Growth age at 

Species tolerance rate death 

Fagus grandifolia 5 2 300 

Juniperus scopulorum 1 2 250 

Larix laricina 1 3 150 

Larix occidentalis 1 2 700 

Nyssa aquatics 2 4 80 

Pinus banksiana 1 4 80 

Pinus contorts 2 2 120 

Pinus edulis 1 1 350 

Pinus jeffreyii 2 3 400 

Pinus ponderosa 2 3 600 

Pinus resinosa 1 4 200 

Pinus strobus 2 2 200 

82 

Percent 

system 

domination 

Outbreak 

folivore species 

so 

70 

80 

70 

90 

80 

80 

50 

80 

70 

90 

so 

Heterocampa guttivita 

Halisidota argentata subalpina 

Coleophora laricella 

Pristiphora erichsonii 

Semiothisa sexmaculata 

Zeiraphera improbana 

Malacosoma disstria 

Choristoneura pinus 

Dasychira pinicola 

Neodiprion pratti banksianae 

Neodiprion swainei 

Argyrotaenia tubulana 

Choristoneura lambertiana 

Coleotechnites milleri 

Coleotechnites starki 

Coloradia pandora 

Neodiprion burkei 

Neodiprion nanulus contortae 

Neodiprion educolis 

Coloradia pandora 

Coloradia pandora 

Neodiprion gillettei 

Neophasia menapia 

Parorgyia grisefacta 

Phaeoura mexicanaria 

Zelleria haimbachi 

Neodiprion lecontei 

Diprion similis 
APPENDIX 3 continued 

Host plant parameters 

Average 

Shade Growth age at 

Species tolerance rate death 

Pinus taeda.e 2 4 100 

Pinus virginiana 2 3 100 

Populus tremuloides 1 5 70 

Prunus serotina 2 4 100 

Pseudotsuga menziesii 2 4 7SO 

Quercus alba 2 3 300 

Quercus douglasii 2 2 100 

Quercus ellipsoidalis 2 2 80 

Quercus gambelii 2 2 90 

Quercus garryana 2 2 300 

Quercus lobata 2 4 200 

Quercus rubra 3 4 200 

83 

Percent 

system 

domination 

Outbreak 

folivore species 

70 

80 

80 

so 

so 

so 

70 

so 

n.a. 

n.a. 

70 

so 

Neodiprion excitans 

Neodiprion taedae linearis 

Neodiprion pra.tti pra.tti 

Choristoneura conflictana 

Malacosoma. californicum fragile 

Malacosoma disstria 

Operophtera. bruceata 

Phyllocnistis populiella 

Lithocolletis ontario 

Sciaphila. simplex 

Hydria prunivora.ta 

Ma.la.cosoma americanum 

Choristoneura. occidenta.lis 

Galenaria consimilis 

Nepytia freemani 

Nepytia phantasmaria. 

Orgyia pseudotsugata 

Xylomgyges simplex 

Zeiraphera hesperiana 

Melanolophia. imitata 

Heterocampa. manteo 

Symmerista canicosta 

Malacosoma constrictum 

Archips semiferanus 

Lambdina punctata 

Lambdina fiscellaria somniaria 

Phryganidia californica 

Diapheromera. femorata 
APPENDIX 3 continued 

Host plant parameters 

Average 

Shade Growth age at 

Species tolerance rate death 

Quercus spp. 3 3 lSO 

Robinia pseudoacacia 2 4 60 

Taxodium distichum 3 2 600 

Thuja occidental is 4 2 300 

Tsuga heterophylla s 3 400 

84 

Percent 

system 

domination 

Outbreak 

folivore species 

so Malacosom8 disstria 

Alsophila pometaria 

Anisota senatoria 

Archips argyrospilus 

Caliroa spp. 

Lymantria dispar 

70 Odontota dorsalis 

so Anacamptodes ephyraria 

Archips argyrospilus 

so Argyresthia thuiella 

so Acleris gloverana 

Ectropis crepuscularia 

Epinotia tsugana 

Epirrita autumnata omissa 

Halisidota argentata 

Lambdina fiscellaria lugubrosa 

Neodiprion tsugae 
VARIATION IN THE NUTRITIONAL PHYSIOLOGY 

OF TREE-FEEDING SWALLOWTAIL CATERPILLARS 

MATTHEW P. AYRES, JANICE L. BOSSART, and J. MARK SCRIBER 

Department of Entomology 

Michigan State University 

East Lansing, MI 48824 U.S.A 

INTRODUCfiON 

A key problem in addressing patterns of interaction between forest insects and their host trees is 

determining the level at which important ecological and evolutionary interactions occur. We commonly 

view plant-herbivore relations as herbivore species interacting with plant species, tacitly assuming that 

variation among members of either species is small and one can represent their interaction by the 

average characteristics of the insect and the tree species (Ehrlich and Raven 1964, Feeny 1976, 

Rhoades and Cates 1976, Scriber and Feeny 1979). This simplistic view is violated if insects within a 

species differ markedly in their ability to grow on a particular host, or if trees within a species differ 

substantially in quality as perceived by the insect. If variation within both insect and host species is 

large and pervasive, then insect-plant interactions may be best studied at the level of genotypes and 

populations (Edmunds and Alstad 1978, Fox and Morrow 1981, Thompson 1988a, Ng 1988, Karban 

1989). Clearly intraspecific variation exists. For example, potato beetles, checkerspot butterflies, 

tortoise beetles, autumnal moths, and tiger swallowtails are each comprised of populations that differ in 

their ability to use key hosts (Hsiao 1978, Rausher 1982, 1984, Haukioja and Hanhimaki 1985, Scriber 

1986a, Hare and Kennedy 1986). Likewise mountain birch, cottonwood, honeylocust, and a variety of 

other trees are comprised of populations that differ in their suitability for specific herbivores (Hanover 

1980, Haukioja and Hanhimaki 1985, Pakash and Heather 1986, Herms et al. 1987). Even within 

populations, individual trees may be highly variable (Edmunds and Alstad 1978, Whitham and 

Slobodchikoff 1981, Smiley et al. 1985, Ayres et al. 1987, Whitham 1989). The emerging problem is to 

quantify variation within and between populations relative to variation at other levels. 

Our studies have addressed variation in the nutritional physiology of tree-feeding swallowtail 

caterpillars (Papilionidae: Lepidoptera). A central objective has been to determine the level at which 

ecological and evolutionary divergence has occurred. For example, physiological adaptation of 

caterpillars to their host plants may occur at the level of genotypes and populations, at the level of 

species and species groups, or both. Genetic variation within and between populations implies a 

potential for adaptation to local conditions. Alternatively, substantial variation between closely related 

species, with little intraspecific variation, implies that adaptive shifts occur via reproductive isolation 

and are often associated with speciation events (Mayr 1963). In this case, it is appropriate to 

emphasize species attributes. 

Our research has concentrated on traits of likely ecological importance, and especially on traits 

subject to geographically variable selective pressures. In addition to nutritional physiology and 

detoxification, these include mate choice and reproductive allocation (Burns 1966, Svard and Wiklund 

1986, Lederhouse et al. 1989), cold hardiness and diapause biology (Shimado 1988, Hagen and Scriber 

BARANCHIKOV, Y.N., MATI'SON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

85 
1989, Kukal et al. in prep.), host choice and oviposition behavior (Grossmueller and Lederhouse 1985, 

1987, Thompson 1988b, 1988c, Bossart and Scriber in prep.), and larval temperature responses (Scriber 

and Lederhouse 1983, Ritland and Scriber 1985). Our ability to draw inferences about the evolutionary 

history of these attributes is strengthened by the existence of a large number of Papilio taxa with 

differing degrees of relatedness (Hagen and Scriber 1990). Here we describe recently completed 

experiments testing the nature and extent of variation within two closely related species of Papilio, 

P. glaucus, and P. canadensis. 

BACKGROUND 

Nearctic Tree-feeding Swallowtails 

Most of the common tree-feeding papilionids in North America belong to two sister clades 

within the genus Papilio: the P. glaucus and P. troilus species groups. Host use patterns in the 

P. troilus group are typical of the Papilionidae in that all its members (P. troilus L, P. palamedes 

Drury, and P. pilumnus Boisduval) are restricted to hosts from a single plant family (Lauraceae). In 

contrast, all six members of the P. glaucus group (P. glaucus L., P. alexiares Hoppfer, P. canadensis 

R & J, P. eurymedon Lucas, P. rutulus Lucas, and P. multicaudatus Kirby) feed on more than one 

family of hosts (Scriber 1973, 1984). Polyphagy appears to be a derived trait (synapomorphy) within 

the P. glaucus group (Scriber et al. 1991). Unlike the P. troilus group, neonate larvae of the P. glaucus 

group typically initiate feeding on virtually any foliage they encounter, toxic or not (Scriber et al. 

1991 ). This behavioral difference may have been a critical precondition for the evolution of polyphagy 

in P. glaucus and its relatives because selection cannot screen for suitable physiologies unless the larvae 

feed (Feeny 1991). All members of the P. glaucus group share the ability to feed on black cherry 

(Prunus serotina, Rosaceae) and chokecherry (Prunus virginiana), but P. glaucus species differ in their 

growth performance on most host taxa other than Prunus (Scriber et al. 1991 ). P. eurymedon appears 

to be uniquely capable of developing on Rhamnus (Rhamnaceae). P. canadensis, P. eurymedon, and 

P. rutulus generally grow well on plants of the Salicaceae, yet few P. glaucus or P. alexiares survive 

beyond the first instar. Magnoliaceae are typically lethal to all P. glaucus taxa except P. glaucus and 

P. alexiares. 

Papilio glaucus and Papilio canadensis 

' Best known among the tree-feeding swallowtails are two taxa formerly regarded as subspecies, 

but now believed to be separate species (Hagen et al. in prep.). The transition zone between 

P. glaucus (= "glaucus") and P. canadensis (= "canadensis," formerly P. g. canadensis) coincides with a 

complex ecotone that runs through central Wisconsin and Michigan and extends eastward through 

northern Pennsylvania, central New York, and southern New England (Scriber 1988). The ecotone has 

long been recognized as the transition between boreal coniferous forests and diverse deciduous 

southern forests (Curtis 1959, Braun 1974). This zone marks a climatic boundary between regions 

influenced by cool, dry air masses to the north and warmer, wetter air masses to the south; it 

approximates the 1,400 degree day isotherm (100 C base), which is the lower limit for bivoltine 

potential in glaucus (Scriber 1988). The ecotone also corresponds to the southern edge of Pleistocene 

continental glaciation and thus marks a discontinuity in soil types, topography, and history of occupancy 

by plants and animals. 

P. glaucus and P. canadensis are distinguishable by wing morphology, allozymes, and 

mitochondrial DNA restriction sites (Luebke et al. 1987, Hagen 1990 and in prep.). They also differ 

in several characteristics of obvious ecological significance. Diapause is induced by short photoperiods 

in the multivoltine glaucus, while canadensis is necessarily univoltine (Rockey et al. 1987a, 1987b). The 

species also differ in the expression (y-linked trait in glaucus) and suppression (x-linked trait in 

86 
canadensis) of a mimetic dark morph in the females (Clarke and Sheppard 1962, Hagen and Scriber 

1989). Host use differences between glaucus and canadensis are especially pronounced (Fig. 1). In 

laboratory trials, first instar glaucus larvae grew rapidly on tuliptree, Liriodendron tulipifera, foliage 

(Magnoliaceae), doubling their weight in less than a day, while comparable development in canadensis 

larvae required 3 to 4 days. P. glaucus larvae also grew somewhat faster on hop tree, Pte lea (Rutaceae ). 

Yet on Populus tremuloides (quaking aspen) and Betula papyrifera (paper birch), canadensis larvae grew 

substantially faster than glaucus larvae. These patterns are consistent with those based on first instar 

survival, total development time, and pupal mass (Scriber 1983, Lindroth et al. 1986). The 

northernmost limits of tuliptree and hoptree, and the southernmost limits of aspen and birch, are 

coincident with the transition zone between the species. However, glaucus and canadensis range limits 

are not a simple consequence of these host distributions because other common hosts for each, e.g. 

cherries (Prunus) and ashes (Fraxinus), extend either side of the transition zone. 

Laboratory handpairings of glaucus and canadensis adults produced F1 hybrids that grew and 

survived on both aspen and tuliptree foliage (Scriber 1986b ), suggesting the involvement of two discrete 

detoxification systems independently controlled by autosomal loci. The ability of canadensis larvae to 

use quaking aspen depends at least in part on the ability to detoxify phenolic glycosides (Lindroth et 

al. 1988, Scriber et al. 1989). Backcross studies indicated a detoxification threshold necessary for 

survival, beyond which performance on diets containing phenolic glycoside tremulacin increased with 

increasing proportions of canadensis genes. 

Intraspecific Variation 

Populations of glaucus and canadensis in different regions may encounter very different 

communities of host plants. This is true on a relatively fine scale (river valleys versus uplands) as well 

as on a coarser geographic scale (the swamp bayheads of Florida versus the Appalachian forests of 

southern Ohio, or the northern hardwoods of the Great Lakes region versus the boreal forests of 

interior Alaska). Populations inhabiting regions as distant and floristically disparate as Florida and 

Ohio, or Alaska and the Great Lakes, must be subject to selection favoring physiological traits that 

improve growth performance on local hosts. Indeed, larvae from southern Florida survived better on 

sweetbay, Magnolia virginiana, the only regionally abundant host, than larvae from other glaucus 

populations (Scriber 1986a ). It has been suggested that Florida populations of P. glaucus represent a 

distinct race, P. g. australis Maynard, but electrophoretic comparisons indicate no barriers to gene flow, 

and we regard the Florida insects as southern populations of P. glaucus. 

The remainder of this paper describes experiments designed to test the prevalence of regional 

specialization (Hsiao 1978, Scriber 1983, Scriber 1986a) and allow for quantitative comparisons of 

variation within and between populations with variation between species and species groups. One set 

of experiments compares canadensis populations from Alaska and the Great Lakes region. Other 

experiments compare glaucus populations from Florida, Georgia, and Ohio. Associated electrophoretic 

studies provide estimates of population divergence and substructuring independent of the growth 

performance studies and survey specific allozymes for linkage with host-use abilities. 

87 
....... 

-I 

'"C 

-I 

0) 

E 

. 

C) 

E 

'-""" 

0.8 

0.6 

w 0.4 

~ a: 

:::t: 

~ 0.2 

0 

c: 

" 0.0 

11 P. canadensis AK 

Eil P. canadensis Ml 

~ P. glaucus Ml 

95o/o Cl 

Populus Betula Llrlodendron Ptelea 

MICHIGAN HOST SPECIES 

1 

w 

:E 

i= 

2 (!' 

z 

:::i 

CD 

4 ~ 

0 

8 c 

16 

Figure 1. Relative growth rate of first instar larvae from three insect 

populations tested on four Michigan host species. Right hand axis shows the 

time required for larvae to double their weight at the corresponding growth 

rate. The insect populations are P. canadensis from Alaska, P. canadensis 

from northern Michigan, and P. glaucus from southern Michigan. The host 

species, from left to right, are Populus tremuloides (quaking aspen), Betula 

papyrifera (paper birch), Liriodendron tulipifera (tuliptree), and Ptelea 

trifoliata (hoptree). The experiment was conducted from 13 to 20 June 1988 

using leaves collected from Ingham County, Michigan. Error bars indicate 

95 percent confidence intervals. 

METHODS 

Butterfly Collection and Oviposition 

Adult females were captured from populations in Florida, Georgia, Ohio, Michigan, Wisconsin, 

and Alaska, then transported on ice or shipped using overnight delivery to our laboratory for 

oviposition. Females were placed in clear plastic boxes (10 em x 20 em x 27 em) with sprigs of 

appropriate foliage, held at 100 percent humidity under artificial illumination ( 4 hr dark alternating 

with 4 hr light), and fed a honey-water solution daily. Eggs were collected every other day, and 

resulting neonate larvae were used for the laboratory growth performance studies. 

88 
Electrophoresis 

Butterflies were frozen at -800C to preserve tissues for allozyme electrophoresis. Four 

polymorphic allozyme loci were examined using thin-layer cellulose acetate plates. Alleles were named 

according to their relative mobility, with the most common P. glaucus allele assigned the value of 100; 

negative numbers were assigned to cathodally migrating allozymes. Detailed techniques are described 

elsewhere (Hagen and Scriber 1989, Bossart in prep.) 

Larval Performance of P. canadensis 

We compared P. canadensis populations from interior Alaska (Fairbanks and vicinity) and the 

Great Lakes region (northern Wisconsin and the Upper Peninsula of Michigan), 4,000 km away. Some 

studies also included interspecific comparisons with glaucus larvae from southern Michigan and Ohio 

(500 to 1,000 km from the Michigan canadensis sites). We challenged the larvae with nine host species 

native to Alaska and nine host species native to the Great Lakes region. Of the Great Lakes hosts, 

none of the nine species and only two of the five families are sympatric with Alaska swallowtails. The 

Alaska tree species included the only two hosts regularly encountered by both populations (Populus 

tremuloides and Populus balsamifera) plus seven other species of Salix, Betula, and Alnus, which are 

encountered naturally only in Alaska. We had only limited knowledge of canadensis host use in 

Alaska, so we chose species likely to be hosts based on their distribution and taxonomy. In the first 

summer we documented natural use of four out of the nine species: Populus tremuloides, Populus 

balsamifera, Alnus tenuifolia, and Salix novae-angliae (Scriber and Ayres 1990). 

Our standard measure of growth performance was first instar relative growth rate. The same 

protocol was used for experiments conducted in Fairbanks, Alaska, and East Lansing, Michigan. Each 

population was represented on each host by 17 to 20 larvae drawn from 5 to 8 full-sib families. 

Larvae from the two populations hatched at the same time and were tested concurrently on the same 

sample of leaves. Leaves were collected as the canadensis eggs began to hatch. Each host species was 

represented by leaves from five genetically distinct trees. Freshly hatched larvae were weighed, then 

distributed singly to clear plastic vials containing foliage from one of the experimental hosts. A 

moistened plaster-of-paris base in each vial provided high humidity and maintained leaf turgor 

throughout the trial. Nearly all larvae fed on the foliage offered them. After 2 days (24°C, 

photoperiod of L:D 18:6), the larvae were reweighed. A typical larva weighed 1.5 mg at hatch (T 1) 

and, on a good host, 6.2 mg at T f· Final weights were reduced by 10 percent ( = estimated weight of 

food in their gut) to make them comparable to initial weights (taken before the larvae had begun to 

feed). Relative growth rate was calculated as (ln(W f) - ln(W 1))tr, where W f equals the final weight, 

W 1 equals the initial weight, and T equals the time in days (Gordon 1968, Ayres and MacLean 1987). 

Degrees of freedom for population comparisons were based on the number of families. 

Larval Performance of P. glaucus 

We compared P. glaucus populations from Lawrence County, Ohio, Clarke County, Georgia, and 

Highlands County, Florida, on three hosts: Liriodendron tulipifera, Magnolia virginiana, and Prunus 

serotina. These populations span 1,300 km, each separated from the nearest population by about 650 

km. The three experimental hosts are all used naturally by P. glaucus and support generally high levels 

of growth performance. The frequency of use differs between populations. Florida P. glaucus are 

largely restricted to Magnolia virginiana, the only common host throughout much of peninsular Florida. 

In contrast, Georgia and Ohio populations rarely or never encounter Magnolia virginiana. A variety of 

host species occur in Ohio and Georgia, but the Ohio population probably encounters Liriodendron 

more frequently than other hosts and the Georgia population probably encounters Prunus most 

frequently. 

89 
In 1988 progeny from 6 Florida families, 8 Ohio families, and 14 Georgia families were reared 

individually in plastic petri dishes (24°C, photoperiod of L:D 18:6). Ten neonate larvae from each 

family were randomly allocated to each of the three hosts. Liriodendron and Prunus leaves were 

collected every other day from trees near East Lansing, Michigan. Magnolia leaves were collected from 

trees maintained in our greenhouses. Larvae were reared to adults. Larval duration, pupal mass, and 

sex were recorded. Similar experiments were conducted in 1989. Population comparisons may have 

been somewhat confounded by seasonal changes in the foliage because the natural phenology of the 

populations differed and we were unable to rear the larvae synchronously. 

RESULTS AND DISCUSSION 

Variation within P. canadensis 

Relative growth rates on nine Wisconsin tree species ranged from 0.61 mg-mg- 1-d -1 on 

Betula nigra to 0.20 mg-mg-1.d -1 on Betula allegheniensis (Fig. 2). These rates correspond to 

doubling times of 1.1 versus 3.5 days, respectively, indicating a broad spectrum of host quality. Overall, 

the Alaska and Great Lakes insect populations did not differ: least square means ± 1 SE equalled 

0.425 ± 0.029 versus 0.414 ± 0.039 mg-mg-1.d -1 for Alaska and Wisconsin respectively (P = 0.81). 

The contrast between populations was not significant for any of the nine hosts treated separately (P > 

0.05). These results counter predictions of the regional specialization hypothesis. A match between 

the physiological attributes of Wisconsin caterpillars and the nutritive characteristics of Great Lakes 

hosts might have arisen through the acquisition of new abilities in the Wisconsin population (e.g. a 

detoxification and digestive system suitable for basswood) or the loss of ancestral and unneeded 

abilities in the Alaska population. There is no evidence that either of these processes has occurred for 

any of the host taxa examined. 

The reciprocal comparison between canadensis larvae from Alaska and Wisconsin on nine Alaska 

host species revealed a similar pattern (Fig. 3). There was a weak overall tendency for Alaska 

canadensis to grow faster than Wisconsin canadensis (least square means ± 1 SE equalled 0.525 ± 0.029 

versus 0.458 ± 0.019 mg-mg-1.d-1 for Alaska and Wisconsin respectively, P = 0.06). But Alaska 

larvae also tended to grow slightly, though not significantly, faster on Wisconsin hosts. The contrast 

between canadensis populations was significant for only one of nine Alaska hosts (Salix glauca, t = 

3.44, df = 13, P < 0.01). We do not interpret these modest effects as evidence of local adaptation to 

host characteristics. The most general test for the hypothesized pattern of local specialization to 

regional hosts was the ANOVA interaction between canadensis populations (Alaska and Wisconsin) and 

host community (nine Alaska host species and nine Wisconsin host species), which was insignificant 

(P = 0.43, F = 0.64, df = 1, 20). The test for interactions between host species and families within 

populations was also insignificant (P = 0.99, F = 0.74, df = 160, 357). Yet these were robust tests 

involving 696 larvae and 18 host species; given the observed variance, we had a high probability of 

detecting any ecologically meaningful differences. Far from being a mosaic of differentiated populations 

and variable genotypes, the host-use abilities of P. canadensis appear to be remarkably constant across 

a broad geographic range. 

In contrast to the absence of variation within or between canadensis populations, there was a 

marked difference between canadensis and glaucus. First instar growth rates of P. glaucus from Ohio 

were 34 percent lower overall when tested on the same Alaska host species (Fig. 3). On all nine hosts 

considered separately, the mean growth rate of glaucus larvae was lower than both canadensis 

populations, and on six of the nine hosts, the contrast between species was significant (P < 0.05). 

Only on Salix alaxensis, Salix bebbiana, and Betula resinifera did glaucus larvae grow at rates 

approaching that of canadensis larvae. The two swallowtail species seem fundamentally different in 

their ability to feed on a broad array of boreal host plants. 

90 
II P. canadensis AK 95°/o CJ 

Em P. canadensis WI 

....-. 

..... 0.8 I 

-c 1 ,......._ 

0 ..... I > C') as 

E 0.6 , 

......... . 

C') w E :E ........ - w 0.4 t1-

<( 2 ~ 

c: z 

- :I: -I 

1- 0.2 m 

3: 4 :::J 

0 0 8 c a: 

" 1 6 

0.0 

arner vir ser gran amer pap nig all rug 

-- -- Tilia Populus Betula 

Prunus Fraxinus Alnus 

WISCONSIN HOST SPECIES 

Figure 2. Relative growth rate of first instar P. canadensis from Alaska and 

Wisconsin on nine Wisconsin host species. The host species, from left to 

right, are Tilia americana (basswood), Prunus virginiana (chokecherry), Prunus 

serotina (black cherry), Populus grandidentata (bigtooth aspen), Fraxinus 

americana (white ash), Betula papyrifera (paper birch), Betula nigra (river 

birch), Betula allegheniensis (yellow birch), and Alnus rugosa (speckled 

alder). The experiment was conducted from 5 to 8 July 1989 using leaves from 

Dunn County, Wisconsin. Error bars indicate 95 percent confidence intervals. 

First instar growth rates are just one measure of growth performance, but we have found them 

to be a powerful and generally reliable index. As part of a larger study (Ayres and Scriber in prep.), 

the 360 canadensis larvae initiated on Alaska hosts (Fig. 3) were reared to pupation and additional 

measurements collected. These data support our conclusion based on neonate performance that the 

populations do not differ in their nutritional physiology. Relative growth rates measured over the 

middle ins tars (day 3 to 17) did not differ between populations, nor did fifth ins tar growth rates, 

consumption rates, or conversion efficiencies. Hosts that produced high first instar growth rates tended 

to have higher overall survival and yield larger pupae in less time than hosts that produced low first 

instar growth rates. Larger pupae produce larger male and female adults that produce larger 

spermatophores and more eggs respectively (Leder house et al. in prep.). 

The apparent absence of variation in detoxification systems and nutritional physiology is in 

contrast to other traits that do vary between the populations. Alaska females produced eggs 150 

percent larger than their Great Lakes counterparts, but were able to produce only 63 percent as many 

91 
,... 

t 

C) 

E 

. 

C) 

E .._... 

0.8 

0.6 

0.4 

0.2 

0.0 

li P. canadensis AK 

EiJ P. canadensis WI 

~ P. g/aucus OH 

95o/o Cl 

trem bals a/ax bebb glauc nov resin crisp ten 

Populus Salix Betula Alnus 

ALASKA HOST SPECIES 

1 

2 

4 

8 

1 6 

-

1-

" z 

-...1 

m 

::l 

0 

c 

Figure 3. Relative growth rate of first instar larvae from three insect 

populations tested on nine Alaska host species. The insect populations are 

P. canadensis from Alaska, P. canadensis from Wisconsin, and P. glaucus from 

Ohio. The host species, from left to right, are Populus tremuloides (quaking 

aspen), Populus balsamifera (balsam poplar), Salix alaxensis (feltleaf 

willow), Salix bebbiana (bebb willow), Salix glauca, Salix novae-angliae, 

Betula resinifera (Alaska paper birch), Alnus crispa (green alder), and Alnus 

tenuifolia (thinleaf alder). The canadensis measurements were made from 26 to 

29 June 1988 and the glaucus measurements from 19 to 22 August 1989; all 

leaves were collected from the same sites near Fairbanks, AK. Error bars 

indicate 95 percent confidence intervals. 

as Wisconsin females of equal size (Leder house et al. in prep.). These larger eggs conferred an 

important developmental advantage. At 17 days after hatch, the Alaska canadensis larvae were still 1.5 

times larger, even after a 180-fold increase in weight (relative growth rates were virtually identical) 

(Ayres and Scriber in prep.). Further, Great Lakes larvae tended to grow for a longer period and 

consequently produced larger pupae, even though they hatched smaller and grew at the same rate. The 

populations further differed in their larval temperature responses. In particular, Alaska larvae were 

capable of more rapid growth and development at the relatively low temperatures of 12° and 18°C 

(Ayres in prep.). 

92 
z 

0 

t= 

< a: 

::> 

c 

_. 

< 

> a: 

< _. 

32 

30 

28 

26 

24 

m P. g/aucus FL 

D P. glaucus GA 

l2a P. glaucus OH 

Prunus Magnolia Liriodendron 

HOST SPECIES 

Figure 4. Larval duration of P. glaucus populations from Florida, Georgia, 

and Ohio tested on Prunus serotina (black cherry), Magnolia virginiana 

(sweetbay), and Liriodendron tulipifera (tuliptree). Measurements were made 

during May, August, and September 1988 for Florida, Ohio, and Georgia 

populations respectively. Error bars indicate 95 percent confidence 

intervals. 

Variation within P. glaucus 

Unlike P. canadensis, P. glaucus appears to harbor substantial genetic variation in nutritional 

physiology. Patterns in development time, especially significant interactions between insect populations 

and host species, support the hypothesis of regional specialization (Fig. 4, Table 1 ). Overall, the 

development time of Ohio glaucus tended to be longer than that of Florida glaucus (population effect, 

Table 1), but this difference was most pronounced on Magnolia (the prevalent Florida host) and 

nonexistent on Liriodendron (the prevalent Ohio host, population x host interaction, Table 1 ). 

Likewise, Georgia populations required a longer development time on Magnolia than Florida 

populations, even though development times were identical on Prunus (a prevalent Georgia host, 

Fig. 4). Significant variation among families within populations suggests an even finer level of 

ecological specialization, although the variation within populations was far smaller than that between 

populations (F = 14.95 versus 1.83 for main effects of population and family respectively, and F = 

4.15 versus 1.39 for host x population interactions and host x family interactions respectively, Table 1). 

93 
Table 1. Mixed Model ANOVA (families nested within population) of larval 

duration for three P. glaucus populations tested on three host 

species. Data are shown in Fig. 4. 

Source of Error 

variation df MS terma F p 

Population 2 134.41 Fam(Pop) 14.95 < 0.001 *** 

Host 2 308.66 H x F(Pop) 45.32 < 0.001 *** 

Family(Pop) 25 8.99 Error 1.83 < 0.05 * 

Host x Pop 4 28.23 H x F(Pop) 4.15 < 0.01 ** 

Host x F(Pop) 54 6.81 Error 1.39 < 0.05 * 

Error 315 4.91 

a Mean square used as denominator in F test (Ayres and Thomas 1990) 

Further evidence for local adaptation lies in the relationship between larval duration 

(development time) and pupal mass. On Magnolia, Florida families with long development times 

tended to produce larger pupae (Fig. 5); this result is to be expected if all families grow at similar 

rates (are uniformly well adapted), but vary in the timing of pupation. In contrast, the negative 

correlation between larval duration and pupal mass of Ohio families feeding on Magnolia suggests 

differential detoxification abilities among families. For example, larvae from relatively maladapted 

families may partially have compensated for their low growth rates by extending the duration of growth, 

but the prolonged development time was inadequate to produce pupae of equal mass. On 

Liriodendron, Ohio families with relatively long development times tended to produce larger pupae, as 

expected for a population well adapted to Liriodendron (r = 0.31, P = 0.16). There was no relation 

between development time and pupal mass for Florida families on Liriodendron (r = -0.06, P = 0.86), 

indicating a mix of the two patterns. 

Visual inspection of reaction norms further supported a physiological tradeoff 

(genotype-environment interaction) in the ability of full-sib families to use Liriodendron and Magnolia 

(Fig. 6). Within both Ohio and Florida populations, families with rapid development on Magnolia 

took relatively longer on Liriodendron. The tradeoff between performance on Liriodendron and 

Magnolia appears linked to the presence of particular glucosephosphate isomerase (GPI) alleles 

(Table 2). Within each population, homozygous GPI1001100 genotypes tended to be fast growers on 

Liriodendron and heterozygous GPI1001_104 genotypes tended to be fast growers on Magnolia 

(Bossart in prep.). Moreover, the frequency of the GPI _104 allele tended to be higher in Florida, 

where Magnolia is the prevalent host (Table 3). We are currently unable to distinguish between 

genetic linkage and physiological causality as the basis for this relationship. No fixed differences in 

allozymes have been found between the populations, and the suggested clinal patterns were not 

statistically significant. 

94 
........ 

C) 

-

en 

en 

<( 

:E 

..J 

<( 

c. 

~ 

c. 

1.8 

1.6 

1.4 

1.2 

1.0 

• P. g/aucus FL 

o P. g/aucus OH 

• 

• 

r = 0.64 

= 0.01 

eQb--e.. <(9 

........ 0 

o oo --................ 0 

0 0 0 ---.... 0 0 --.... 

• 

0 

0 r = -0.38 

p = 0.08 

0.8~------T---~~~~~~~~~~~----~ 

22 26 30 34 38 42 

LARVAL DURATION (days) 

Figure 5. Relationship between larval duration and pupal mass of P. glaucus 

from Florida and Ohio reared on Magnolia virginiana. Each point represents 

the mean of 3 to 30 full-siblings. Figure includes data from 1988 and 1989. 

Table 2. Larval duration of different glucosephosphate isomerase (GPI) 

genotypes from Florida and Ohio tested on Magnolia virginana and 

Liriodendron tulipifera. Values are mean± SE (N). The interaction 

between host and genotype was significant at P- 0.0008 (F- 12.15, 

df = 1, 76). 

Florida 

Ohio 

Liriodendron 

GPI100/100 GPI100f-104 

22.36 ± 0.45 

(11) 

23.88 ± 0.44 

(16) 

26.75 ± 0.75 

(8) 

27.55 ± 1.14 

(11) 

95 

Magnolia 

GPI100/100 GPI100/-104 

26.06 ± 0.45 

(18) 

29.64 ± 0.95 

(11) 

24.86 ± 0.67 

(7) 

28.50 ± 0.50 

(2) 
z 

0 

i= 

< a: 

::) 

c 

..J 

< 

32 

30 

28 

> 26 a: 

< ..J 

• P. glaucus FL 

---o-- P. glaucus OH 

0 

' 

o,,\\ ±SE ! 

' ' ' ' ' ' ' ' ' ' o,. ' ' ', ', ~ .......... ~.::::-~--' ' ........... ,, ... ;:-.... ' ....... ~~ ~.:"----

........ ~' ~- ----o '\.~ '---... , ' ' ' 

24+-------~--------------~------

Magnolia Liriodendron 

HOST SPECIES 

Figure 6. Larval duration of P. glaucus families from Florida and Ohio tested 

on Liriodendron tulipifera and Magnolia virginiana. Each point represents the 

mean of 6 to 10 full-siblings. Lines show family reaction norms. Standard 

error associated with family means is indicated (SE2 - MSError/N -/4.91/5). 

CONCLUSIONS 

P. canadensis appears to be a recently evolved taxon derived from a glaucus-like ancestor 

(Scriber et al. 1991, Hagen and Scriber 1990). Our results suggest that the detoxification systems and 

nutritional physiology of ancestral canadensis became greatly modified in ways that allowed them to 

exploit a diversity of northern hosts. In the process, some ancestral abilities were lost (e.g. tulip tree 

detoxification) and others were retained (e.g. hoptree detoxification). The absence of detectable 

differentiation between widely separated canadensis populations encountering very different hosts 

suggests that the nutritional physiology of canadensis has remained largely unchanged since its 

divergence from a glaucus ancestor. The absence of detectable variation within canadensis populations 

implies that future changes in nutritional physiology will be limited by the appearance of new 

mutations. Its implied history of rapid evolutionary change followed by stasis is consistent with the 

stepwise mechanism of herbivore adaptation described by Ehrlich and Raven (1964). We note, 

however, that direct reciprocal evolutionary responses by the hosts are unlikely because of the low 

levels of damage inflicted by these herbivores. In striking contrast, P. glaucus appears to be a vast 

complex of differentially adapted genotypes and populations, which suggests that its nutritional 

physiology is being shaped by local selective pressures such as result from varying regional availability 

of hosts. The polyphagous habits of P. glaucus are enhanced by its variability within and between 

populations, which is not so for P. canadensis, all genotypes of which appear equally capable of using 

any host species within its range. 

96 
Table 3. Allele frequencies (%) at four polymorphic loci in P. glaucus 

populations from Ohio (OH), Georgia (GA), and Florida (FL). Number 

of alleles per sample - 48 to 84. 

Population 

Locus Allele OH GA FL 

PGM 91 3 1 0 

94 4 1 4 

97 12 29 16 

100 35 30 36 

103 38 27 28 

106 8 11 16 

109 0 1 0 

IDH-2 100 83 92 71 

102 17 8 25 

103 0 0 4 

MPI 90 3 0 0 

92 0 3 0 

94 0 11 13 

96 16 14 11 

98 22 29 20 

100 47 32 51 

102 12 11 5 

GPI -105 3 0 0 

-104 7 12 21 

100 79 78 75 

104 1 0 0 

105 7 10 4 

We suggest several possible explanations for the markedly different levels of intraspecific 

variation within glaucus and canadensis. 1) The two species differ in population structure such that 

gene flow is more restricted in glaucus than canadensis. 2) P. canadensis originated as a very small 

population, perhaps as a result of Pleistocene isolation in some periglacial refugium (Scriber 1988), and 

low variation is a result of the associated genetic bottleneck. 3) P. canadensis is of such recent 

evolutionary origin that populations have not yet differentiated, but will in the future. 4) There is less 

variation in canadensis host use; perhaps Populus tremuloides is the prevalent host for all canadensis 

populations, and other host-use records are rare "oviposition mistakes" that contribute only 

insignificantly to selective pressures shaping the nutritional physiology of canadensis. 5) The boreal 

forest is characterized by low phytochemical diversity relative to that of temperate forests, the most 

ubiquitous boreal hosts being restricted to four genera in two families: Populus, Salix, Betula, and 

Alnus. Consequently, natural selection has favored the development of a single detoxification system 

that is optimal for most hosts, i.e. canadensis detoxification systems have been canalized such that 

mutations and recombination seldom lead to phenotypic variation. 

97 
Hypothesis 1 can be tested by comparing the divergence in allozyme frequencies between 

populations within species. If it holds true, the fixation index (Fsr) of glaucus populations should be 

greater than that of canadensis populations separated by the same geographic distance. The available 

data are limited, but they indicate extensive gene flow within both species (Hagen 1990); the estimated 

genetic distance between P. glaucus from Ohio and Florida was no greater than that between 

P. canadensis from Alaska and Michigan: Nei's genetic identities equalled 0.99 in both cases (Hagen 

and Scriber 1990). Hypotheses 2 and 3 cannot account for divergence between canadensis populations 

in traits other than nutritional physiology such as egg size, adult size, and temperature responses. 

Hypothesis 2 would be supported by lower levels of allozyme heterozygosity in canadensis than in 

glaucus (Bonnell and Selander 1974). Hypothesis 3 predicts that other recently derived swallowtail taxa 

(as estimated from allozyme and mtDNA sequence divergence) would be similarly invariant in their 

nutritional physiology. Hypothesis 4 questions our view of P. canadensis as a polyphagous herbivore 

and requires that suitable hosts go generally unused. It can be tested through quantification of 

oviposition patterns in the field. We presently favor hypothesis 5, which predicts that the various 

secondary metabolites present in boreal hosts are detoxified by canadensis using only one or a few 

biochemical systems. It further predicts that other polyphagous herbivores of tqe boreal forest will 

similarly exhibit low variation in nutritional physiology, and will be consistently less variable than 

related species of polyphagous herbivores from temperate and tropical forests (Mattson et al. 1988, 

Mattson et al. in this volume). An important correlate is that physiological preadaptation to 

alternative hosts will be more common in boreal forests than elsewhere. That is, boreal herbivores 

challenged with sympatric nonhost plant species should be more likely to successfully detoxify that 

foliage than temperate or tropical herbivores challenged with nonhost species from their environment. 

ACKNOWLEDGMENTS 

We acknowledge the ideas and insightful suggestions shared by John Bryant, Guy Bush, Robert 

Hagen, Don Hall, Dan Herms, Kelly Johnson, Robert Lederhouse, Stephen MacLean, William Mattson, 

Jim Miller, and James Nitao. Bruce Ayres, Darsie Ayres, Ed Debevic, Robert Lederhouse, and Doozie 

Snyder assisted with the experiments. The manuscript was greatly improved by Stephen MacLean. 

Laboratory space, logistical support, and intellectual stimulation were generously provided by the 

Institute of Arctic Biology, University of Alaska, Fairbanks. Research was supported by the National 

Science Foundation (BSR 87-18448 and BSR 88-01184), USDA Competitive Grants (87-CRCR-1-2581), 

Michigan State University (MAES Project #8051, AURIG), and a Sigma Xi award. 

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102 
DO DIFFERENCES IN INDUCIBLE RESISTANCE 

EXPLAIN THE POPULATION DYNAMICS 

OF BIRCH AND PINE DEFOLIATORS? 

SEPPO NEUVONEN and PEKKA NIEMELJ\1 

Department of Biology 

University of Turlru 

SF-20500 Turku, Finland 

The Finnish Forest Research Institute 

Department of Forest Protection 

P.O. Box 18, SF-01301 Vantaa, Finland 

INTRODUCTION 

Damage inflicted by insects may trigger responses in their host plants resulting either in 

immediate effects on herbivores either rapidly or in effects upon subsequent herbivore generations. 

Differentiation between rapid and delayed inducible resistance is essential since the two responses affect 

the population dynamics of herbivores in fundamentally different ways (Haukioja 1982). Rapid 

inducible resistance (RIR) tends to stabilize herbivore population dynamics. On the other hand, 

delayed inducible resistance (DIR) introduces a time-lag into the negative feedbacks regulating the 

population dynamics of insects and may generate cyclical fluctuations in density (Benz 1974, Haukioja 

1980, Berryman et al. 1987). 

Experiments have shown that rapid and/or delayed inducible resistance exists in some 

tree-herbivore systems while other systems apparently lack such responses (Haukioja and Neuvonen 

1987). The variation in inducible responses may help us to understand differences in the population 

dynamics of defoliators on different host trees. For example, both white birch (Betula pubescens) and 

Scots pine (Pinus sylvestris) suffer large-scale defoliation in Fennoscandia. Howc;wer, the outbreaks on 

birches and pines show different temporal and geographic patterns. This paper compares inducible 

resistance mechanisms and patterns in the population dynamics of defoliating insects Scots pine and 

birch. 

DEFOLIATING INSECfS ON SCOTS PINE AND BIRCH 

Scots pines and birches are abundant and widespread in northern Europe. Thus the species 

richness of insects feeding on these trees is great (Larsson and Tenow 1980, Neuvonen and Niemeli 

1983), though, only some of the insects cause serious damage to their host. The most important 

defoliators of Scots pine in Fennoscandia (Neodiprion sertifer and Diprion pint) belong to the sawflies 

(Symphyta: Diprionidae) (Table 1). In other areas, however, such as Central Europe and Siberia, these 

1order of authorship determined by tossing a coin. 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

103 
are also lepidopteran species (Bupalus piniarius, Panolis jlammea, Dendrolimus pini) which can become 

predominant defoliators of pine. 

The mountain birch forests in northwestern Europe are periodically defoliated by geometrid 

larvae feeding mainly during the early season (Table 1). Several species (Epirrita autumnata, 

Operophtera spp., and Erannis defoliaria) fluctuate greatly and fairly synchronously in density (Tenow 

1972, Haukioja et al. 1988). Local defoliations may also be caused by a late season sawfly, Dineura 

virididorsata (Koponen 1981 ). 

OUTBREAK PA1TERNS 

Birch-Feeding Insects 

An extensive record of geometrid defoliation of Fennoscandian birch forests has been compiled 

over the years from 1862 to 1968. During this span of time outbreaks have occurred at 9- to 10-year 

intervals (Tenow 1972). The duration of these outbreaks is short, 2 to 3 years. Distribution of the 

outbreaks shows a number of varying patterns. Outbreaks of Epirrita autumnata are restricted to the 

mountain birch forest zone of northern Finland and the Scandinavian mountain chain. In the birch 

forests along the Norwegian coast, Operophtera spp. are the most important defoliators, and 

E. autumnata occurs mainly at higher altitudes and at inland localities with a more continental climate 

(Tenow 1972). Outbreaks of Operophtera spp. and Erannis defoliaria have been recorded on isolated 

islands in the southwest archipelago of Finland (Tenow 1972, Laasonen and Laasonen 1987). Birches 

are also regularly defoliated in other areas of the world, e.g. Rheumaptera hastata on Betula resinifera 

in Alaska (Werner 1981). 

Furthermore, defoliation by Epirrita larvae is often topographically restricted, patches of 

undefoliated birch forests typically occur at the bottom of river valleys while birches at higher altitudes 

are usually heavily defoliated (Kallio and Lehtonen 1973, Tenow 1975). 

Pine-Feeding Insects 

In Fennoscandia outbreaks of diprionid sawflies are restricted chiefly to southern regions and 

are, with few exceptions, absent from northern areas (Christiansen 1970, ~yttyniemi et al. 1979, 

Juutinen and Varama 1986). Diprionid outbreaks on pine are not cyclical as are the well-known 9-year 

cycles of the tortricid, Zeiraphera diniana, on European larch (Baltensweiler et al. 1977, Hans.ki 1987, 

Geri 1988). In Sweden and Finland local outbreaks of diprionids occur every year (Larsson and Tenow 

1984, Juutinen and Varama 1986). Large-scale outbreaks occur irregularly in 10- to 20-year intervals 

(Kangas 1963, Hanski 1987). 

The duration of outbreaks in a given habitat is variable. According to Juutinen and Varama 

(1986), outbreaks of N. sertifer last 3 to 4 years in southern Finland. In the middle region of Finland 

the duration is 4 to 6 years. In the SaariselkA mountain chain in northern Finland, an outbreak has 

been chronic for the last 20 years (Juutinen 1967, Juutinen and Varama 1986). 

N. sertifer outbreaks in Fennoscandia and in parts of the U.S.S.R. characteristically occur 

following dry summers and are restricted mainly to dry sites or dense stands (Juutinen 1967, Larsson 

and Tenow 1984, Sharov, this volume). Interestingly, several successive large-scale outbreaks of 

N. sertifer occurred during the warm period in the 1930s (Kangas 1963, Hanski 1987). 

Defoliations by other insect pests in Fennoscandia are more sporadic than those caused by 

N. sertifer. In more southern areas of Europe, such as Germany and some parts of Britain, some 

populations of Bupalus piniarius and Panolis flammea show more or less regular cycles of 6 to 11 years 

(Schwerdtfeger 1968, Barbour 1987), while other populations are relatively stable or fluctuate 

irregularly, e.g. most British populations (Barbour 1988). 

104 
Table 1. Outbreak species of Scots pine (Pinus sylvestris) and birches 

(Betula pendula and B. pubescens) in Fennoscandia 

Species 

Neodiprion sertifer 

Diprion pini 

Gilpinia pallida 

Hicrodiprion pallipes 

Bupalus piniarius 

Epirrita autumnata 

Operopthera spp. 

Erannis defoliaria 

Dineura virididorsata 

Scots pine 

Family 

Diprionidae 

Diprionidae 

Diprionidae 

Diprionidae 

Geometridae 

Birches 

Geometridae 

Geometridae 

Geometridae 

Tenthredinidae 

Larval period 

May-July 

July-September 

June-August 

June-August 

June-August 

May-July 

May-July 

May-July 

July-September 

EXPERIMENTAL EVIDENCE OF INDUCffiLE RESISTANCE 

Experiments on Birch 

Rapid Inducible Resistance 

Mechanically damaged birch foliage is less suitable for the growth of larvae of several 

lepidopteran and hymenopteran species than undamaged control foliage (Haukioja and NiemeUl 1977, 

1979, HanhimH.ki 1989). Larvae grew for a longer time and the pupal masses were the same or lower 

on damaged than on control foliage (Table 2). When the total impact of RIR on the capacity of 

E. autumnata to increase were estimated by combining the effects on survival and fecundity, the 

reduction ranged from 0 to 22 percent (Haukioja and Neuvonen 1987). Rapid inducible resistance 

against E. autumnata seems to be equal in birch provenances from both outbreak (northern Finland) 

and nonoutbreak (southern Finland) areas (Haukioja and HanhimH.ki 1985). 

Rapid inducible resistance in birch foliage can be triggered by damaging early, but not lateseason birch leaves (Haukioja and Niemela. 1979, Wratten et al. 1984). However, the responses may 

have such a long relaxation time that they also affect insects feeding later that season (Neuvonen et al. 

1988, HanhimH.ki 1989). On the other hand, not all types of damage to birch trees result in 

deterioration in foliage quality. Increased densities of insects have been observed on birches browsed, 

either artificially or by moose, during the previous winter(s) (Danell and Huss-Danell 1985), though the 

performance of Epirrita larvae was affected only slightly (Neuvonen and Danell 1987, Haukioja et al. 

1990). 

105 
Table 2. The existence of rapid (RIR) and delayed induced resistance (DIR) on 

mature Scots pine needles and birch foliage (see Haukioja and 

NiemelA (1979) and HanhimAki (1989) for more examples). 0- no 

statistically significant effect, + significant increase, 

- significant decrease. Some statistical tests may suffer from 

sacrificial pseudoreplication. Damage on Scots pine needles 

occurred during mid or late season (for the effects of early season 

damage, see Neuvonen et al. 1988). 

Development/ Pupal Larval 

Insect species growth rate weight survival References* 

Scots pine needles 

RIR 

Neodiprion sertifer + 0 + 1 

Gilpinia virens 0 0 0 1 

Microdiprion pallipes 0 0 1 

Diprion pini 0 0 0 1 

DIR 

Neodiprion sertifer 0 0 0 1 

Diprion pini 0 +/0 -/0 10 

Birch foliage 

RIR 

Epirrita autumnata 0 2,3,4 

Dineura virididorsataa 0 0 0 3,5 

DIR 

Epirrita autumnata 6,7,8 

Dineura virididorsataa + ? ? 9 

*References: 1) NiemelA et al. (1984), 2) Haukioja and NiemelA (1977), 

3) Haukioja and NiemelA (1979), 4) Haukioja and HanhimAki (1985), 5) Neuvonen 

et al. (1988), 6) Haukioja et al. (1985), 7) Haukioja and Neuvonen (1985), 

8) Neuvonen et al. (1987), 9) Neuvonen (pers. observ.), and 10) NiemelA (pers. 

observ.). 

British experiments have concentrated on reporting chemical changes induced by foliage damage 

and their effects on the feeding preferences of herbivores (Wratten et al. 1984, Hartley 1988, Hartley 

and Lawton 1991 ). These studies have shown the existence of RIR, as evidenced by increases in 

phenolics, in British birch provenances, although the feeding bioassays have yielded variable results. 

Some British studies have also reported negative effects of foliage damage on the performance of 

insects (Bergelson et al. 1986, Fowler and MacGarvin 1986). 

106 
Delayed Inducible Resistance 

Decreased quality of foliage during years following simulated or real insect attack, or delayed 

inducible resistance, can be triggered by mechanically damaging the birch leaves or by depositing feces 

of Epirrita larvae beneath/at the base of the birches (Haukioja et al. 1985). Insect damage induces a 

stronger delayed inducible response than does manual damage (Hauldoja and Neuvonen 1985, 

Neuvonen et al. 1987). Both survival of Epirrita larvae and pupal weights were reduced on defoliated 

trees (Table 2). Performance, as measured by combined effects on survival and fecundity, of 

E. autumnata on partially defoliated trees may be over 70 percent below that on control birches. 

Mountain birches which had been artificially defoliated 2 to 4 years earlier still caused a reduction of 

16 to 38 percent in fecundity (Hauldoja and Neuvonen 1987). Birch provenances outside the usual 

outbreak range of defoliating insects may not express DIR (Haukioja 1980, Haukioja et al. 1983), and 

it is difficult to say whether this is a cause or a consequence of the distribution of outbreaks. 

The foliage of defoliated mountain birches has lower nitrogen and higher phenolic content than 

that of control trees in the years following damage (Tuomi et al. 1984). Because of the high negative 

correlation between nitrogen and phenolic concentrations in birch foliage, it is difficult to evaluate 

which of these factors is more important in determining the success of Epirrita larvae. However, when 

the nitrogen content of birch foliage has been accounted for in models explaining variation in the 

pupal weight of Epirrita, the additional contributions of phenolic content have not appreciably 

improved the explanatory power of the models (Haukioja et al., unpubl. observ. ). 

Experiments on Pines 

Studies of 20- to 25-year-old Scots pines in Finland have suggested that neither RIR nor DIR 

apparently develops in the mature foliage, the normal diet of diprionid sawflies (NiemelA et al. 1984). 

For example, four sawfly species survived and grew equally well on mature needles from control and 

defoliated (in the spring of the same and in previous years) branches. Geri et al. (1990) reached 

nearly the same conclusions working in France on the sawfly, Diprion pini. But, surprisingly, they 

discovered that female fecundity declined substantially on previously but not concurrently defoliated 

trees even though all other performance parameters (survival, growth, developmental rates, diapause 

rates) showed little response to defoliation. This is evidence for DIR, but not RIR. Because NiemelA 

et al. (1984) did not measure fecundity, which is usually positively correlated with insect growth, it is 

not known whether this performance variable declined due to defoliation. However, Sharov (this 

volume) found no changes in the fecundity of Diprion pini during outbreaks on Scots pine in the 

Rostov region of the U.S.S.R., as would be expected if there were strong DIR responses in pine. 

In the case of other evergreen conifer species and other defoliators, there is some evidence for 

either weak RIR or DIR (Wagner and Evans 1985, Leather et al. 1987, Wagner 1988, Mattson et al. 

1988). The study of Thielges (1968) has often been cited, though incorrectly, as an example of induced 

resistance. What he actually observed, however, was only that an "abnormal compound" occurred in 

the foliage of Scots pine heavily damaged by N. sertifer. It is not possible to evaluate whether this 

compound resulted from defoliation or existed prior to it, nor whether it was harmful to the larvae. 

We conclude that there is at best only a weak DIR in Scots pine. Otherwise, one should be 

able to measure significant reductions in insect growth, developmental rates, and survival, none of 

which has been found. 

HYPOTHESES EXPLAINING INDUCffiLE RESISTANCE 

Owing to fundamental physiological differences between deciduous and evergreen coniferous trees 

(Dickson 1989), one would expect differences in their defensive responses to folivores. Tuomi et al. 

107 
(1988) suggested that the plants' carbon-nutrient balance (sensu Mattson 1980, Bryant et al. 1983) 

could largely determine the nature of the DIR occurring in the foliage. For example, an increase in 

resistance is expected when defoliation causes a relatively greater deficiency of minerals than carbon--

leading to enhanced carbon-based secondary metabolism. This is presumably the case for deciduous 

trees growing on nutrient-deficient soils and having large carbon reserves in their stems and roots. On 

the other hand, for evergreens, old needles serve both as important sources of carbon reserves, and 

current photosynthates (Bryant et al. 1983), and hence their removal by herbivores may cause a 

relatively greater carbon than nutrient deficiency and hence suppress accumulation of carbon-based 

secondary metabolism. Furthermore, defoliation tends to increase the N content of the needles in 

evergreen conifer trees (Piene 1980, Piene and Percy 1984, UngstrOm et al. 1990) which supports the 

thesis of a defoliation-induced carbon shortage. However, chronic, severe defoliation may eventually 

cause substantial rootlet mortality and result in a serious mineral deficiency thereby leading to 

enhanced secondary metabolite buildup. 

Though differences in the effects of first defoliations on the plants' relative carbon/nutrient 

balance may explain differences in DIR in evergreen and deciduous trees, it is not sufficient to explain 

their apparent differences in RIR. Moreover, bioassays conducted with mountain birch have yielded 

results either difficult to predict from or inconsistent with the carbon/nutrient balance hypothesis 

(Haukioja and Neuvonen 1985, Haukioja et al. 1985). The facts that intensification of DIR is caused 

by cues from insects and that fertilization does not mitigate delayed inducible resistance triggered by 

manual defoliation are more consistent with a view of the responses as actual defenses against 

defoliators. 

Although the carbon/nutrient balance hypothesis cannot explain all the details of delayed 

inducible resistance in birch, it is possible that the incidental responses suggested by it may have 

become truly more defensive in areas where heavy defoliations occur. 

INDUCIBLE RESISTANCE AS A FACTOR IN THE POPULATION DYNAMICS 

OF PINE AND BIRCH DEFOLIATORS 

The apparent absence of strong DIR in mature needles of Scots pine may explain why diprionid 

sawfly outbreaks can continue for several years in the same stands (Juutinen 1967, Juutinen and 

Varama 1986) and why several successive outbreaks are possible (Kangas 1963). Furthermore, the 

apparent lack of regular cycles in the population dynamics of diprionid sawflies is consistent with the 

lack of delayed negative feedbacks via foliage quality. 

Some populations of pine defoliators show more or less regular cyclical fluctuations (Barbour 

1988). It seems probable that other delayed feedback mechanisms than inducible changes in foliage 

quality are involved in these cases. The existence of DIR in those pine provenances has to be tested 

before any firm conclusions are possible, however. 

As compared with other possible regulating factors, the importance of DIR is well established in 

birch/herbivore systems showing cyclical fluctuations in insect densities (Haukioja et al. 1988). These 

responses introduce time-lag negative feedback into the population dynamics of Epirrita. The 

importance of RIR is far less clear, on the other hand. D IR may be a key factor in the cyclical 

density fluctuations of birch defoliators in some areas, though this does not obviate the importance of 

other factors (e.g. parasitoids, diseases). DIR also contributes to the relatively short duration of 

Epirrita outbreaks. 

108 
SUMMARY 

Both the presence and the absence of induced resistance in tree foliage can explain the 

population dynamics of defoliating insects. White birch (Betula pubescens) and Scots pine (Pinus 

sylvestris) suffer large-scale defoliation in Fennoscandia. Outbreaks of birch defoliators have occurred 

at 9- to 10-year intervals. Duration of the outbreaks is short, 2 to 3 years. On Scots pine, local 

outbreaks occur every year, and large-scale outbreaks follow irregularly in 10- to 20-year intervals. 

That DIR produces time-lag negative feedback in the population dynamics of herbivores can explain 

the cyclical fluctuations. The absence of inducible responses in the mature foliage of Scots pine may 

explain why outbreaks can continue for several years in the same stands and why several successive 

outbreaks are possible. 

ACKNOWLEDGMENTS 

We thank Erkki Annila, Sinikka Hanhimltki, Erkki Haukioja, and William Mattson for critical 

comments and helpful discussions. 

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112 
REPEATED DAMAGE OF LEAVES 

BY PHYLLOPHAGOUS INSECfS: 

IS IT INFLUENCED BY RAPID INDUCIBLE RESISTANCE? 

I.A BOGACHEVA 

Institute of Plant and Animal Ecology 

Ural Branch of the U.S.S.R. Academy of Sciences 

8 March Street 

202 Sverdlovsk 620144 U.S.S.R. 

INTRODUCTION 

It was discovered more than 10 years ago that toxic and repelling substances may increase in 

plant tissue in response to damage by phyllophages. Such rapidly inducible chemical changes may 

appear a few hours after leaf injury and then disappear in a few weeks or months (Walker-Simmons 

and Ryan 1977, Baldwin and Schultz 1983, Van Hoven 1974, Wratten et al. 1984). This phenomenon 

has been investigated in detail on mountain birch, Betula pubescens tortuosa, in Finland (Haukioja and 

Niemeli 1977, 1979, Niemela. et al. 1979, Haukioja 1982, Neuvonen and Haukioja 1991). Research 

there has. demonstrated that consumption of leaves from damaged shoots has detrimental effects on the 

development, fecundity, and sometimes the survival of several species of insects. The same adverse 

effects were found for insects feeding on damaged willow (Raupp and Denno 1984), larch (Niemela. et 

al. 1980), and other trees and shrubs. Although these effects may easily be demonstrated in laboratory 

and field tests, it is not clear what role they play in phyllophage population dynamics (Fowler and 

Lawton 1985). Are they a real defense against herbivores? If there are damage inducible defenses in 

plant leaves, it is reasonable to suppose that phyllophagous insects may have evolved mechanisms for 

coping with or rejecting damaged leaves. For example, laboratory trials have clearly shown that 

polyphagous lepidopteran larvae prefer to feed on intact birch leaves (Wratten et al. 1984). Arguments 

for the benefits of rapid inducible resistance (RIR) in plants are not so convincing. They emphasize 

the increased dispersion of insect injuries within a tree crown and the subsequent increase in mortality 

of the insects (Edwards and Wratten 1983, Silkstone 1987). However, this effect has been shown to be 

weak, and in many cases was not found at all (Silkstone 1987). Moreover, some laboratory 

experiments have shown that phyllophages are not capable of distinguishing damaged leaves and hence 

of avoiding them (Raupp and Denno 1984, Hartley and Lawton 1987). 

I have investigated the effects of RIR on leaf choice by folivorous insects in Subarctic and 

southern taiga forests. In the Subarctic, different species of folivorous insects co-occurred on birch 

leaves more often than would have been expected according to the Poisson (random) distribution 

(unpubl. data). Initially, feeding wounds by chewing and sucking insects were distributed independently 

among leaves, but subsequently damaged leaves were more frequently and intensively attacked by insects 

than intact leaves. However, parallel observations made the same year in the southern taiga zone of 

the Urals gave quite different results. Co-occurrence of folivorous and sucking insects was more rare 

than expected according to the Poisson distribution, and some folivorous insects avoided certain leaf 

damage patterns (Bogacheva 1989). What is the reason for such a discrepancy between two different 

geographic regions? Why did we fail to demonstrate an over-dispersion of subsequent insect damage in 

BARANCHIKOV, Y.N., MA'ITSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

113 
the Subarctic? What are the main factors in leaf preference by phyllophagous insects: qualitative 

changes in damaged leaves or ecological conditions of leaf environment? In this paper I address these 

questions both in the field and in the laboratory (food choice experiments). 

EXPERIMENTAL METHODS 

Field Experiments 

Experiments similar to those by Silkstone (1987) were done in 1988 at two sites: in forest 

tundra (66° 40'N) at the Labytnangi field station in the Low Ob' region, and in southern taiga (56° 

SO'N) near the city of Sverdlovsk in the Middle Urals. Around Labytnangi we worked with the Betula 

pubescens ssp. tortuosa growing in the small groves. Near Sverdlovsk we worked with Betula pubescens, 

the most common tree species in this region. I defoliated growing leaves using a 0.5 em cork borer. 

One leaf from each intact dwarf shoot was so damaged, amounting to 3 to 4 percent of the mean leaf 

area on dwarf shoots. This was equal to the mean value of natural leaf consumption in the Subarctic, 

but in Sverdlovsk the mean consumption level averages 2 to 3 times higher. 

I administered three kinds of treatments: 1) making one hole on one side of the leaf lamina, 

leaving the leaf margin undamaged (hereafter referred to as "middle hole"); 2) making two holes on 

one side of a leaf, but along the leaf margin, their total area and perimeter similar to those of the 

"middle hole" (this damage pattern hereafter referred to as "marginal holes"); and 3) keeping intact 

leaves as a control. All three leaves formed one replicate; they were similar both in size and in their 

position on a branch. Leaves were marked with dots of type-correction fluid. We used 20 replicates 

per tree, and there were 25 study trees at Labytnangi, 26 at Sverdlovsk. Unfortunately, some leaves 

were lost during the course of the experiments, 3 weeks at Labytnangi (6/30/88 - 7 /24/88) and over 

3 months at Sverdlovsk (5/27 /88 - 9/12/88), i.e. until leaf fall. At the end of the experiments, mines 

and holes made in the leaves by insects were classified according to the list of 15 types of feeding 

damage earlier described (Bogacheva 1984). Amount of injury was measured using graph paper. 

Frequency distribution patterns of the damage size classes for each different damage type were 

compared using Chi-square tests. Galls found on leaves were recorded, but were rare; feeding injury by 

sucking insects was not recorded. 

Laboratory Tests 

We conducted laboratory tests at the Labytnangi field station in 1988 using the geometrid, 

Epirrita autumnata Bkh., and the weevil, Phyllobius maculatus Tourn. These two experimental insects 

were reared in the laboratory at room temperature (17 to 25°C) and natural photoperiod. Solitary 

insects were kept in Petri dishes on a damp filter paper. 1\vo damaged and two intact leaves were 

placed in each dish daily. Each pair of leaves was similar in size and position within the tree crown, 

and all of the leaves used for each experimental series were collected from one birch tree. Only intact 

leaves from intact dwarf shoots were used. We artificially damaged one leaf in each pair 1 to 3 days 

before the experiments by creating the "middle hole" of the above-mentioned size. The food was 

changed every 24 hours and the amount of leaf lamina eaten was measured using graph paper. For 

weevils, the total number of feeding holes and their position within a leaf were also registered. Only 

last instar larvae were used in trials. Epirrita autumnata were very abundant in 1988, so they were 

changed every day or every two days during the experiments in order to rule out possible influence of 

individual induced preference. Weevils, on the other hand, were not abundant and thus were changed 

only in case of death or feeding refusal. In total, 53 specimens of geometrid larvae and 18 specimens 

of beetles were used; leaves for them were collected from 6 and 4 different birch trees, respectively. 

114 
RESULTS 

Field Experiments 

Only four birch leaves were lost in the field experiment at Labytnangi. Since incomplete 

replicates were excluded from the calculations, we had a total of 496 rather than 500 replicates 

(Table 1). 

At Sverdlovsk a large number of leaves was lost and many replicates became incomplete so the 

calculations were carried out in two ways: 1) only on complete replicates, of which there were 347, 

and 2) on all the leaves of each treatment, including those of incomplete replications. Owing to the 

larger sample size (Table 2), more data appeared to differ significantly when the second method was 

used. However, the mean value of the data did not change considerably. 

There were no differences among treatments at Labytnangi (Table 1 ). At Sverdlovsk, on the 

other hand, there were significant differences among treatments (Table 2). The data suggest that insect 

responses to the two patterns of artificial damage were not equal: insects apparently avoided leaves 

with marginal holes, preferring leaves with middle holes. Although these two damage patterns differed 

significantly from one another, neither differed significantly from the control (Table 2). 

It is not clear why these two damage patterns are of different attractiveness for phyllophages 

despite the fact that the areas and perimeters of the holes are similar in both cases. One likely 

explanation is the differential detection of damaged leaves by insects using leaf blade shape outlines. 

Thus different positions of grazings on leaf blade surfaces appeared to cause different insect reactions. 

As for insect reactions to damaged leaves, they were found to be different at Labytnangi and 

Sverdlovsk, but, again, the reasons are not clear. Feeding damage of type 2 (large holes on leaves) is 

caused by insects of several families (many lepidopterans, some species of Tenthredinidae and 

Curculionidae species). At Labytnangi feeding injuries of this type are caused mainly by spring species 

of Epirrita autumnata, while at Sverdlovsk they are caused mainly by summer species of Iepidoptera and 

Tenthredinidae. Feeding injuries of type 4 (small skeletonized spots on the underside of leaves) were 

caused by one summer tenthredinid species at Labytnangi and mainly by one late summer species of 

the Coleophoridae family at Sverdlovsk. Finally, feeding marks of type 7 (the tortuous grazings at leaf 

edge) were caused by Polydrusus weevils at both sites, though clearly by different species. 

In summary, there were no differences in insects' responses to damaged and intact leaves at 

Labytnangi, but such differences did occur at Sverdlovsk, where insects were apparently attracted to 

leaves with middle holes and repelled by those with marginal damage. The latter damage pattern 

predominates in nature and our results thus run contrary to current theory, which predicts avoidance of 

all damaged leaves. Contrary to our results, on the other hand, Silkstone (1987) reported that middle 

lamina injuries decreased further insect damage. The reasons for this discrepancy will be discussed 

later. 

Laboratory Tests 

Under the conditions of our experiment, Epirrita autumnata larvae fed equally on both damaged 

and intact birch leaves (Table 3), while Phyllobius beetles preferred damaged leaves (Table 4). This 

suggests that different phyllophagous species may have different reactions to damaged leaves. 

115 
Table 1. Percent leaf damage and area of insect consumption per damaged leaf 

(mm2) on Betula pubescens ssp. tortuosa trees in the field 

experiment at Labytnangi 

T r e a t m e n t 0 f 1 e a v e s 

Types of Leaf damage (%) and Middle hole Marginal holes Control 

damage a consumption (mm2 ) A B c 

General Damage (%) 52.5 46.9 46.9 

Consumption 17.3 13.3 15.2 

Type 2 Damage (%) 7.3 5.1 3.8 

Consumption 74.9 59.9 100.8 

Type 4 Damage (%) 1.2 5.3 3.2 

Type 7 Damage (%) 44.4 41.8 43.2 

Consumption 7.3 7.0 6.8 

Total leaves 496 496 496 

aType 2 - large holes; type 4 - small skeletonized spots; type 7 - tortuous 

grazings at leaf edge (for details see Bogacheva 1984, and discussion in 

text). 

Why should different species have different responses? First, taxonomically different species may 

have different chemoreceptors. Second, moths feed on leaves during the larval stage whereas weevils 

feed at the adult stage, and in that sense they are ontogenetically different. Third, rapidly induced 

responses may have different effects depending on the ecological peculiarities of insects (Edwards and 

Wratten 1983, Wratten et al. 1984). Both species involved here are considered generalists. In the Low 

Ob' region, I found Epirrita caterpillars feeding on mountain birch, Betula nana, Alnus fruticosa, Salix, 

Populus tremula, Rosa acicularis, and Lonicera coerulea. In the same region, I found Phyllobius 

maculatus on mountain birch and alder only, so, at that site at least it appears to be oligophagous. 

Finally, food choice may depend on insect mobility (Schultz 1983, Neuvonen and Haukioja 1991 ). The 

mobility of the two test species is also different: in 24 hours the weevils usually "travel" throughout an 

entire birch crown, Epirrita larvae only within a single branch, as a rule. This difference in mobility 

has been observed in experiments as well: Epirrita caterpillars damaged only two (1.81 ± 0.09) of four 

leaves available in Petri dishes, as a rule, inflicting four (x = 4.18 ± 0.40) holes. Phyllobius specimens 

often damaged all four leaves available (x = 3.21 ± 0.09), inflicting about nine (x = 9.88 ± 0.47 

holes). 

116 
Table 2. Percent leaf damage and area of insect consumption per damaged leaf 

(mm2) on Betula pubescens trees in the field experiment at 

Sverdlovsk 

T r e at m e n t 0 f 1 e a v e s 

Types of Leaf damage (%) and 

damage consumption (mm2) A-1 B-1 C-1 A-2 B-2 C-2 

General Damage (%) 42.7 36.0 41.2 45.0 35.2 41.6 

Consumption 53.0 30.2 39.4 51.4a 29.8b 41.4 

Type 2 Damage (%) 10.1 9.5 8.7 9.5 8.6 8.6 

Consumption 184.3a 73.2b 127.8 200.5b 72.8a 133.6 

Type 4 Damage (%) 18.7 15.0 21.3 20.8 14.7c 22.7b 

Consumption 6.5 7.6 7.3 5.9a 7.7b 7.0b 

Type 7 Damage (%) 18.7 13.5 14.1 17.3 13.9 12.8 

Consumption 8.8 7.1 7.4 8.6 7.1 7.6 

Total leaves 347 347 347 400 397 406 

a, b, and c indicate different treatments (see Table 1); 1 and 2 indicate 

different methods of calculation. Consumption data with different letter 

indexes differ significantly (p ~ 0.05). 

Table 3. Consumption (mm2) of damaged and intact Betula leaves by Epirrita 

larvae 

Tree Days after Damaged Intact Statistical 

number Replicates treatment leaves (mm2) leaves (mm2) significance 

1 8 1 195.62 165.62 n.s. 

2 10 2 179.30 104.00 n.s. 

3 10 3 151.40 191.90 n.s. 

4 10 2 284.80 298.80 n.s. 

5 20 2-3 161.20 146.00 n.s. 

6 9 2 131.67 296.67 n.s. 

Total for all 

experiments 67 1-3 180.85 191.97 n.s. 

117 
Table 4. Consumption (mm2) of damaged and intact Betula leaves by Phyllobius 

weevils 

Tree Days after Damaged Intact Statistical 

number Replicates treatment leaves (mm2) leaves (mm2) significance 

7 20 1-2 50.65 33.95 n.s. 

8 10 1 126.50 43.30 p ~ 0.01 

9 20 1-2 60.70 60.10 n.s. 

10 30 1-3 64.17 40.80 p ~ 0.05 

Total for all 

experiments 80 1-3 68.34 44.22 p ~ 0.001 

Furthermore, the experimental data suggest that different plants elicit different insect responses 

to leaf damage. Weevils showed a clear preference for damaged leaves from trees 8 and 10, but could 

not distinguish between damaged and intact leaves from tree 9 (Table 4). Heterogeneity of plants is 

an important source of variation (Fowler and Lawton 1985, Neuvonen and Haukioja 1985, Neuvonen 

and Haukioja 1991 ). When observing food selection by weevils, I learned that they prefer to begin 

eating at the artificial hole. The number of their feeding marks within 1 em of the marginal hole was 

4 to 5 times greater than that within 1 em of the undamaged leaf edge (weevils' grazings were strictly 

marginal). The presence of the cork borer hole itself seems to account for the attractiveness of 

damaged leaves to weevils. It alone seems to facilitate grazing, although follow-up investigations are 

necessary to confirm this (Gibberd et al. 1988). 

DISCUSSION 

1\vo phyllophagous insects common in the Low Ob' subarctic region did not reject damaged 

leaves in the laboratory tests. Birch insect guilds are represented by dozens of species, but most of 

them are rare. Because I failed to find rejection of damaged leaves in two mobile, spring 

phyllophagous species, I would not expect to find it in summer or in less mobile species. It was not 

surprising that avoidance of damaged leaves was not detected in the field experiments for Polydrusus 

ruficomis Bonsd. (Curculionidae), the most abundant summer species in those sites (Table 1, type 7). 

When analyzing the course of natural leaf damage, I found already damaged leaves more likely to be 

damaged subsequently than the controls. Furthermore, subsequent insect grazing on the damaged 

leaves was more intensive (Bogacheva 1989). 

The same was true for Phyllobius maculatus in laboratory tests at Labytnangi, but in nature this 

species is not the main consumer. One of the latter, E. autumnata, did not distinguish between 

damaged and intact leaves. Comparing my observations in nature with my experimental data, I 

conclude that insect preference for damaged leaves is caused not by leaf attractiveness (as a result of 

damage) but by some other property. All the comparisons were made between leaves from 

brachyblasts within one branch, i.e. with homogeneous plant material Even within a single branch, 

however, some degree of heterogeneity does exist, including genetic fluctuations of defensive substances' 

content (Whitham 1981 ), uncertain variability in foliage feeding quality (Schultz 1983), and different 

light conditions in various twig parts can promote insect feeding on a certain leaves. Temperature 

(lighting of leaves) may be among the main factors determining insect food preference in the subarctic. 

118 
In the southern taiga zone at Sverdlovsk, the avoidance of damaged leaves by phyllophages was 

demonstrated in both laboratory and field experiments (Bogacheva 1989). The avoidance was rather 

weak, however, because the damaged and adjacent leaves were not free from subsequent insect damage. 

How can one explain the differences observed between the two sites? One possible explanation may be 

that in the subarctic forest, differences between damaged and intact leaves are not as important as 

some other factors, particularly ecological ones. In the south taiga, on the other hand, where the 

suppressing effects of low temperatures are eliminated, slight variations in leaf chemistry may be of 

greater importance. Nevertheless it is undeniably true that similar leaf damage patterns are caused at 

two sites by different insect species. However, even closely related species are known (Fowler 1984) to 

have different food preferences. The next step required to obtain an unambiguous explanation is 

experimentation with the same phyllophagous species at the two sites and/or chemical analysis of 

damage-induced leaf alterations. 

With respect to the general significance of rapid inducible resistance against phyllophages, 

integrating my data and those of others, I believe that the pattern of responses by phyllophages to 

damaged-induced changes in leaves varies with many factors. The causes of these differences in 

phyllophages' responses can be classified into three large groups. 1) Given the inherent properties of a 

damaged plant, phyllophages' responses to injured leaves vary depending on (a) plant species (Edwards 

et al. 1986); (b) plant individual within the species (Fowler and Lawton 1985, Neuvonen and Haukioja 

1985, Lawton 1986, Hartley and Lawton 1987, our observations); (c) site conditions (Baldwin 1988); 

(d) leaf age (Haukioja and NiemeUi 1979, Edwards et al. 1986, Hartley and Lawton 1987); and (e) time 

span between damage and subsequent insect feeding (Fowler and Lawton 1985, Edwards et al. 1986, 

Hartley and Lawton 1987). Rapid induced response may be modified by the weather conditions during 

the growing season as well (Haukioja and Hanhimaki 1985); just as it may also modify the insects' 

responses. 2) Given the origin of the primary damage, phyllophages may respond differently if 

(a) primary damage is caused by insects of different ecological feeding modes (folivorous or sucking 

insects, miners, and so on) (Hartley and Lawton 1987); or (b) primary damage occurs within lamina 

position of grazing injury (e.g. middle or marginal wounds, etc.). Doubtless, these differences are 

realized for phyllophages through their host plant. 3) Different responses by phyllophages to similar 

leaf damage patterns are observed (a) in phyllophages of various ecological types, such as folivores, 

sucking insects, miners, and so on (Hartley and Lawton 1987, Neuvonen and Haukioja 1991); (b) in 

specialists and generalists (Edwards and Wratten 1983, Wratten et al. 1984, but see Fowler 1984); 

(c) in phyllophages of different mobility (Schultz 1983, Neuvonen and Haukioja 1991); and (d) at 

different developmental stages of a single phyllophage species which may be connected also with their 

mobility (Harrison and Karban 1986). Finally, in nature coexisting leaves can differ in food quality and 

ecological conditions, i.e. there are conditions both for food choice by insects and for repeated grazings 

on more favorable leaves (Baranchikov 1983, Bultman and Faeth 1985, Fritz et al. 1987, our 

observations). 

Such a diversity of factors influencing responses by insects to damaged-induced leaf change 

enables us to say that the damaged leaf protects itself and adjacent leaves against subsequent injuries 

by only some herbivores. Damaged leaf rejection may be inherent in certain phyllophages species 

feeding on certain host plants. Though it may be possible to find damaged leaf avoidance among an 

entire insect guild on a certain plant, because the guild consists usually of few species, there is no 

justification for extending this response pattern to all plants and all consumers. I propose that the 

avoidance of injured leaves by insects does not exist as a general phenomenon. One can still ask, 

however, whether this effect, when it occurs, is beneficial for a plant. We have already mentioned that 

owing to the adverse effect of damaged leaves on insect performance, damaged leaf avoidance seems to 

be more necessary for insects than for plants. However, it is disputable even for insects. Is it more 

profitable for herbivores to continue feeding on damaged leaves, which retards their development 

(increased mortality due to carnivores and parasites) and decreases their fecundity, or to search for an 

intact leaf, thereby wasting energy (loss of body weight and fecundity) and increasing their chances of 

being detected by their natural enemies? Obviously, we are not ready to answer such a question. 

119 
Hartley and Lawton (1987) have studied the adaptive value of insect rejection of damaged leaves 

from the point of view of individual variability in plant chemistry. They found that foliar phenol 

content was so variable that it was sometimes higher in undamaged leaves than in damaged ones. 

"Hence, avoidance of damage is certainly no guarantee of better foliage quality" (Hartley and Lawton 

1987). It is not surprising, then, that avoidance does not occur in all cases. When we state that a 

damaged leaf protects itself against subsequent damage, we consider the situation in terms of a· leaf, 

though it is not the leaf but the plant that is the system to be protected. Let us consider rapid 

inducible defense in those terms. Increased dispersion of insect grazing throughout the tree crown and 

heightened mortality of phyllophages during their "traveling" in the canopy should not be considered a 

real benefit to plants because they also cause damage to previously intact leaves and may increase the 

fitness of the phyllophages. One can hardly characterize such consequences as a plant defense. I 

hypothesize that the alternate strategy, forcing insects to feed on damaged leaves, protecting the intact 

ones, and thus effecting deterioration of phyllophages' fitness, would be more beneficial to plants. 

Indeed, it requires that damaged leaves be attractive instead of repellent. When discussing rapid 

inducible resistance as a defense against subsequent, more serious damage to the whole plant, Rafes 

(1980, 1981) proposed that after the overall damage level attained a 60 to 70 percent threshold, there 

should follow a significant elevation in general resistance, such that the remaining 30 to 40 percent of 

the leaves would go undamaged. This phenomenon might be really profitable to a plant if it did 

indeed occur. One must consider, however, what would happen if insect feeding were not yet 

completed and the threshold damage level of 60 to 70 percent had been reached. The insect is not 

likely to die because mortality increases rather insignificantly in insects that feed on damaged leaves 

(Haukioja and NiemeUi 1979). Many phyllophagous species are not readily able to change their host 

tree and will thus simply continue to feed. Foliage damage of 80 to 90 percent has often been 

recorded (Dmitrienko 1976, Petrenko and Petrenko 1981, Bogacheva 1989), even at low levels of leaf 

area consumption, to say nothing of the situation during insect outbreaks. Hence it appears that the 

existence of a threshold value of damaged leaves triggering resistance to inhibit subsequent damage is 

not supported by evidence. 

SUMMARY 

It was established earlier that in the Low Ob' region (forest tundra zone), damaged leaves of 

mountain birch received more frequent and more intensive subsequent phyllophages damage than intact 

ones, whereas in the Middle Urals the opposite trend was found. To obviate the factors of ecological 

heterogeneity and inherent leaf variability, field and laboratory experiments were carried out. Field 

studies in the forest tundra zone did not reveal different insect responses to damaged and intact leaves. 

On the other hand, in the south taiga, insects avoided leaves with marginal holes and were attracted to 

those with middle holes. In food choice experiments, neither of two phyllophagous species avoided 

injured leaves; in fact one insect, Phyllobius maculatus, preferred them. Although it is correct to view 

damaged leaf avoidance as a plant defense, one cannot consider it a general phenomenon. 

LITERATURE CITED 

BALDWIN, T.J. 1988. Short-term damage-induced increases in tobacco alkaloids protected plants. 

Oecologia 75: 367-370. 

BALDWIN, T.J. and SCHULTZ, J.C. 1983. Rapid changes in tree leaf chemistry induced by damage: 

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lesnukh nasekomykh. IFW-Press, Krasnoyarsk. (In Russian.) 

120 
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northern boundary of tree vegetation. Sov. Ecolog. Zurnal. 3: 153-159. (In Russian.) 

BOGACHEV A, I.A 1989. Possibilities of repeated food plant's consumption by phyllophagous insects: 

local aspect. Ekologiya 1: 66-72. (In Russian.) 

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EDWARDS, P.J., WRATTEN, S.D., and GREENWOOD, S. 1986. Palatability of British trees to 

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associations of gall-forming sawflies in relation to shoot size on their willow host plants. 

Oecologia 73: 159-169. 

GIBBERD, R., EDWARDS, P.J., and WRATTEN, S.D. 1988. Wound-induced changes in the 

acceptability of tree-foliage to Lepidoptera: within-leaf effects. Oikos 51: 43-47. 

HARRISON, S. and KARBAN, R. 1986. Behavioural response of spider mites (Tetranychus urticae) to 

induced resistance of cotton plants. Ecol. Entomol. 11: 181-188. 

HARTLEY, S.E. and LAWTON, J.H. 1987. Effects of different types of damage on the chemistry of 

birch foliage, and the responses of birch feeding insects. Oecologia 74: 432-437. 

HAUKIOJA, E. 1982. Inducible defenses of white birch to a geometrid defoliator, Epirrita autumnata, 

p. 199-203. Proc. 5th Symp. Insect-Plant Relationships. Wageningen. 

HAUKIOJA, E. and NIEMELA, P. 1977. Retarded growth of a geometrid larvae after mechanical 

damage to leaves of its host tree. Ann. Zool. Fenn. 14: 48-52. 

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occurrence of increased resistance in foliage after mechanical damage of adjacent leaves. 

Oecologia 39: 151-160. 

LAWTON, J.H. 1986. Food-shortage in the midst of apparent plenty? the case for birch feeding 

insects, p. 219-228. Proc. 3rd European Congress Entomology. Amsterdam, Utrecht. 

NEUVONEN, S. and HAUKIOJA, E. 1985. How to study induced plant resistance? Oecologia 

66: 456-457. 

121 
NEUVONEN, S. and HAUKIOJA, E. 1991. The effects of inducible resistance in host foliage on birch 

feeding herbivores, p. 277-292. In Raupp, M.J. and Tallamy, D.W., eds. Phytochemical Induction 

by Herbivores. John Wiley & Sons, New York. 464 p. 

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Damage-induced increase in leaf phenols with trypsin-inhabiting effect. Rep. Kevo Subarct. Res. 

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lepidopteran larvae after mechanical damage to leaves of tamarack and dwarf birch near 

Schefferwille, central Quebec-Labrador peninsula. McGill Subarct. Res. Rep. 30: 52-56. 

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comprehensive characteristic of consortive relations in the forest biogeocenosis, p. 77-79. In The 

role of Insect-Plant Relationship in the Population Dynamics of Forest Pests. Abstr. of papers of 

Soviet participants of IUFROJMAB Meeting. Irkutsk. 

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Biogeocenologicheskoje issledovanie rastitelnojadnykh lesnykh nasekomykh. Nauka, Moscow. 

167 p. (In Russian.) 

RAFES, P.M. 1981. Forest insect-phyllophages interactions, p. 140-202. In ltogi nauki i tekhniki. 

Entomologiya 5, Moscow: VINITI. (In Russian.) 

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beetle, Plagiodera versicola. Ecol. Entomol. 9: 443-448. 

SCHULTZ, J.C. 1983. Habitat selection and foraging tactics of caterpillars in heterogenous trees, 

p. 61-90. In Denno, R.F. and McClure, M.S., eds. Variable Plants and Herbivores in Natural and 

Managed Systems. Academic Press, New York. 

SILKSTONE, B.E. 1987. The consequences of leaf damage for subsequent insect grazing on birch 

(Betula ssp.): a field experiment. Oecologia 74: 149-152. 

VAN HOVEN, W. 1974. Trees' secret warning system against browsers. Custos 13: 14-16. 

WALKER-SIMMONS, M. and RYAN, C.A 1977. Wound-induced accumulation of trypsin-inhibitor 

activities in plant leaves. Plant Physiol. (Bethesda) 59: 437-439. 

WHITHAM, T.G. 1981. Individual trees as heterogenous environments: adaptation to herbivory or 

epigenetic noise? p. 9-27. In Denno, R.F. and Dingle, R.H., eds. Insect Life History Patterns: 

Habitat and Geographical Variations. Springer-Verlag, New York. 

WRATTEN, S.D., EDWARDS, P.J., and DUNN, J. 1984. Wound-induced changes in the palatability of 

Betula pubescens and B. pendula. Oecologia 61: 372-375. 

122 
DOUGLAS-FIR NUTRIENTS AND TERPENES 

AS POTENTIAL FACTORS INFLUENCING 

WESTERN SPRUCE BUDWORM DEFOLIATION 

KAREN M. CLANCY 

USDA Forest Service 

Rocky Mountain Forest and Range Experiment Station 

700 S. Knoles Drive 

Flagstaff, AZ 86001 U.S.A 

INTRODUCTION 

Variation in levels of herbivory within and among plants can be attributed to many mechanisms, 

such as differences in a) host nutritional quality, b) suitability of the physical environment, and 

c) abundance of competitor consumers or natural enemies (Mattson et al. 1982, Denno and McClure 

1983, Mattson and Scriber 1987, Clancy et al. 1988a, 1988b, Mattson et al. 1988). To test the 

hypothesis that variation in host plant nutritional quality is a significant mechanism in plant resistance 

against herbivores, I have selected western spruce budworm, Choristoneura occidentalis (Lepidoptera: 

Tortricidae), and Douglas-fir, Pseudotsuga menziesii, for use as a model system. 

C. occidentalis is one of the most abundant defoliators of true fir and Douglas-fir coniferous 

forests in western North America (Brookes et al. 1987). The larvae preferentially feed on the opening 

buds and the newly developing needles of their host trees. Several lines of evidence suggest that both 

foliar concentrations of nutrients, such as nitrogen, sugars, and minerals, and allelochemicals, terpenes 

in particular, could have important effects on budworm survival and reproduction (Harvey 1974, Kemp 

and Moody 1984, Redak and Cates 1984, Cates 1985, Wagner and Tinus 1985, Cates and Redak 1988, 

Clancy et al. 1988a, 1988b, Wagner et al. 1989, 1990). 

This study was designed, therefore, to compare levels of foliar nutrients (N, sugars, and several 

mineral elements) and allelochemicals (terpenes) between phenotypically "resistant" and "susceptible" 

Douglas-fir trees. Differences in biochemical characteristics between trees that have experienced light 

versus heavy defoliation may provide clues to which nutrients or terpenes are connected with resistance 

to budworm attack. In addition, I compared the results with those from artificial diet experiments that 

were designed to ascertain the budworm's response curves to important host plant nutrients. 

EXPERIMENTAL METHODS 

Field Study 

The study site was a high-elevation, mixed-conifer forest with a history of western spruce 

budworm infestation in the Pike National Forest near Deckers, Colorado. At the time of the study, in 

1988, most of the trees at the site had sustained moderate to severe budworm defoliation for at least 

several years, as determined from their growth form and general condition. 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

123 
I selected 12 resistant trees by identifying mature (at least 20 years old, or well beyond juvenile 

stage) individual Douglas-fir trees with a full crown and good form, as distinct from most of the nearby 

trees that had clearly been defoliated for several successive years. The resistant trees were obviously 

healthy and vigorous and appeared to have sustained little or no defoliation. To pair with each 

resistant tree, I selected a nearby tree (within 30 m) of similar size (height and diameter) and microsite 

(slope and aspect) that was manifestly susceptible to budworm defoliation. 

In late June of the 1988 growing season, corresponding to the late instar feeding period of the 

western spruce budworm, I collected current-year foliage from the 24 study trees for chemical analyses. 

One branch was clipped at random from the mid-crown area of the north, south, east, and west 

quadrants of each tree. All the current-year shoots were immediately removed, bagged, and stored on 

dry ice. The foliage was later transferred to an ultralow freezer and stored at -9QOC until analyzed. 

The needles were pulled off the stems in preparation for the chemical analyses, and a composite 

subsample of all the current-year needles collected from each tree was analyzed. 

Foliage samples were analyzed by the Analytical Services Laboratory of the Ralph M. Bilby 

Research Center, Northern Arizona University, for the following: total Kjeldahl nitrogen and 

phosphorus ( colorimetrically); potassium, calcium, magnesium, and zinc (by flame atomic absorption 

spectroscopy); sugars--including xylose, fructose, glucose, galactose, mannose, sucrose, maltose, lactose, 

and erythrose (by high-performance liquid chromatograph); and terpenes~-28 individual monoterpenes, 

sesquiterpenes, and oxygenated monoterpenes (by capillary column gas chromatograph) (Wagner et al. 

1989). The same procedures were used to analyze nutrient concentrations in artificial diets. 

Data were analyzed using paired t-tests (P s 0.05) to determine whether resistant and 

susceptible trees contained different concentrations of the several nutrients and of terpenes. 

Artificial Diet Experiments 

I evaluated the budworm's response curves to sugars, P, K, Ca, Mg, and Zn using a multiple 

generation bioassay and various artificial diets containing defined levels of the nutrients. My 

experimental base diet had concentrations of N, water, sugars, and most minerals similar to those 

provided by Douglas-fir foliage (Clancy in press). 

I formulated other diets that encompassed the range of mineral (K, Mg, and Ca) and sugar 

concentrations typical for host foliage. However, the P and Zn experiments did not include responses 

at the lower limit because the concentrations of these minerals in the base diet were near the middle 

of the usual range for foliage. 

My insect bioassay procedure measured survival and reproduction for three consecutive 

generations (Clancy in press). The P1 generation of the experiments started with egg masses from my 

laboratory colony of nondiapausing western spruce budworm. Survival rates were determined for three 

periods: early to late larval instars, late instars to pupal stage, and pupal to adult stage. These rates 

were multiplied together to estimate cohort survival to the adult stage. I also incubated egg masses 

produced by the adult moths to determine the proportion that was viable. The bioassay for each 

treatment and generation started with 10 egg masses, which usually produced 200 to 300 first instar 

larvae. At the late instar stage, up to 150 live larvae were transferred to fresh diets to complete larval 

development. From 50 to 120 larvae typically pupated and produced about 40 to 100 moths, which 

laid a total of 25 to 75 egg masses on average. Pupae were weighed and the average female pupal 

mass for each treatment and generation was used to predict fecundity, e.g. the number of oocytes in 

the adult moth (Wagner et al. 1987). Experiments were replicated twice to evaluate repeatability. 

Data obtained from these experiments were used in the following population growth model to 

get a composite measure of the effects on budworm performance of different nutrient levels: 

124 
no. F1 larvae -_(no. P1 larvae) • (P1 % cohort survival to adult stage) • 

(Pl x female fecundity) • (F1 % viable egg masses) 

The number of F 2 and F 3 larvae was calculated using data for the appropriate generation. The model 

estimates the number of first instar larvae alive at the beginning of the F1, F2, and F3 generations, 

assuming that all the treatments in an experiment have equal populations at the beginning of the P1 

generation, i.e. the number of P1 larvae was 1 for all treatments. I plotted the number of F1 to F3 

larvae against the nutrient concentrations for the different treatments in an experiment and determined 

the optimal concentration of each nutrient tested based on the level that produced the most F 3 larvae. 

RESULTS 

The foliage of trees susceptible to western spruce budworm defoliation contained lower levels of 

N (P < 0.001), sugars (P = 0.004), and P (P = 0.009), but higher levels of K (P = 0.018) than that 

of resistant trees (Table 1 ). Foliar concentrations of Ca, Mg, and Zn were not different between 

resistant and susceptible trees (P ~ 0.265) (Table 1 ). 

I also examined ratios of sugars and minerals to N because experimental results had indicated 

that N may determine the amount of food a budworm larva ingests, which in turn affects the amount 

of other nutrients or allelochemicals consumed (unpubl. data). Susceptible trees had higher ratios of 

P, K, Mg,, and Zn to N than resistant trees (P < 0.001) (Table 1) and a tendency toward higher CaiN 

ratios (P = 0.069). The two types of trees did not differ in sugars/N ratios (P = 0.487) (Table 1 ). 

The foliage of susceptible trees had concentrations of sugars and K, plus ratios of P, K, Ca, and 

Zn to N, which were closer to the optimal levels determined by artificial diet experiments than those 

of foliage from resistant trees (Table 1 ). The optimal Mg/N ratio estimated from diet studies was 

between the mean values for resistant and susceptible trees. Levels of P in resistant trees were nearer 

the diet experiment optimum. It should be noted, however, that for sugars, P, P /N, K, and Zn/N the 

optimal diet values either were barely contained in the ranges observed for trees or were outside the 

ranges. Furthermore, none of the optimal diet values would be included in 95 percent confidence 

intervals for average tree values. 

Resistant trees had higher levels of foliar N than susceptible trees, contrary to findings by Cook 

et al. (1978) for Picea glauca and by Piene (1980) for Abies balsamea. I was not surprised at this 

result, however, because experiments conducted with varying levels of N in artificial diets had 

demonstrated that N alone is not a limiting nutrient for C. occidentalis (unpubl. data). 

There were no detectable differences in foliar terpene concentrations between resistant and 

susceptible Douglas-firs (P ~ 0.334) (Table 2). Likewise there was no distinction in total terpene/N 

ratios (P = 0.992) (Table 2). The terpene concentrations were calculated on a fresh mass basis 

because the foliage from all the trees was collected at the same phenological stage and moisture 

contents were thus similar. 

125 
Table 1. Comparison of foliar nutritional chemistry for 12 pairs of Douglasfir trees that appeared to be resistant versus susceptible to 

western spruce budworm defoliation and the optimal concentrations of 

sugars and minerals determined by artificial diet experiments 

Artificial 

Response variablea Douglas-fir foliar chemistr~b diet experiment 

(units) pa Resistant Susceptible optimumc 

N (%) 

X <0.001 1.14 0.93 e 

SE 0.031 0.021 

Range 1.02-1.39 0.80-1.07 

Sug~rs (%) 

X 0.004 11.2 8.9 6.4 

SE 0.43 0.49 

Range 9.5-14.0 5.7-11.9 

Sug~rs/N ratio 

X 0.487 9.9 9.5 5.2 

SE 0.39 0.39 

Range 7.6-12.4 7.1-11.8 

p (~g/g) 

X 0.009 2.03 1.93 3.36 

SE 0.042 0.044 

Range 1.84-2.32 1.71-2.23 

P/N_ratio (x 10) 

X < 0.001 1.78 2.08 2.73 

SE 0.024 0.056 

Range 1.67-1.97 1.71-2.40 

K (~g/g) 

X 0.018 8.89 9.94 12.73 

SE 0.180 0.369 

Range 7.80-9.65 8.16-12.2 

K/N_ratio (x 10) 

X < 0.001 7.85 10.76 10.35 

SE 0.232 0.521 

Range 6.54-9.23 8.08-14.13 

Ca img/g) 

X 0.695 2.78 2.71 3.95 

SE 0.191 0.154 

Range 1.80-4.01 1.91-3.82 

126 
Table 1. Continued 

Response variable& 

(units) 

Ca/~ ratio (x 10) 

X 

SE 

Range 

Mg img/g) 

X 

SE 

Range 

Mg/~ ratio (x 10) 

X 

SE 

Range 

Zn iJJ/g) 

X 

SE 

Range 

Zn/~ ratio (x 1,000) 

X 

SE 

Range 

Douglas-fir foliar chemistryb 

pd Resistant Susceptible 

0.069 

0.265 

< 0.001 

0.631 

< 0.001 

2.49 

0.212 

1.59-3.71 

0.90 

0.030 

0.73-1.07 

0.79 

0.026 

0.68-0.98 

27.8 

0.90 

24-36 

2.44 

0.052 

2.24-2.75 

2.93 

0.188 

2.15-4.29 

0.92 

0.022 

0.80-1.02 

1.00 

0.039 

0.79-1.17 

27.3 

0.53 

24-30 

2.95 

0.084 

2.43-3.30 

Artificial 

diet experiment 

optimumc 

3.21 

1.04 

0.85 

85.6 

6.96 

aAll concentrations are based on the dry mass of the foliage or diet. 

bcurrent-year needles collected in late June 1988, when western spruce 

budworms were in the late-instar feeding period. 

cThe concentration that produced the best budworm survival and 

reproduction when larvae were reared on the diet for three consecutive 

generations. 

dProbability level for a paired t-test comparing foliar chemistry for 

resistant and susceptible Douglas-fir trees, df = 11. 

eExperiments conducted with different levels of N in artificial diets 

demonstrated that responses to N were dependent on levels of minerals in the 

diet. Thus I predict the optimal N concentration will vary according to 

levels of minerals (and other nutrients and allelochemicals) present in the 

food. 

127 
Table 2. Comparison of foliar terpene chemistry for 12 pairs of Douglas-fir 

trees that appeared to be resistant versus susceptible to western 

spruce budworm defoliation& 

Response variable 

Tri~yclene 

X 

SE 

Range 

a-p.!_nene 

X 

SE 

Range 

Cam~hene 

X 

SE 

Range 

,8-p.!_nene 

X 

SE 

Range 

Myr~ene 

X 

SE 

Range 

Menthene-1 

X 

SE 

Range 

Bor~yl acetate 

X 

SE 

Range 

Tot~l monoterpenes 

X 

SE 

Range 

pC 

0.670 

0.495 

0.495 

0.351 

0.920 

0.788 

0.922 

0.334 

128 

Resistant Susceptible 

(~g/g fresh mass) 

84.8 

14.54 

24-165 

367.2 

66.05 

131-795 

544.0 

96.74 

190-1110 

275.3 

66.70 

82-813 

56.9 

8.10 

22-98 

246.1 

32.06 

121-411 

471.2 

81.75 

105-924 

1742.2 

279.52 

590-3347 

77.8 

11.24 

22-171 

321.0 

42.01 

96-643 

471.0 

74.12 

114-1097 

207.5 

36.40 

0-359 

55.7 

9.71 

25-142 

231.1 

44.67 

82-626 

461.5 

85.50 

99-1194 

1411.9 

199.56 

404-3100 
Table 2. Continued 

Response variable 

Total oxygenated monoterpenes 

X 

SE 

Range 

Total terpenes 

X 

SE 

Range 

Total terpenes/N ratio 

X 

SE 

Range 

pC 

0.981 

0.437 

0.992 

Douglas-fir foliageb 

Resistant Susceptible 

(~g/g fresh mass) 

477.4 

84.93 

105-978 

2219.6 

357.62 

775-4325 

ratio x 1,000 

202.1 

35.26 

68.6-408.0 

475.1 

89.67 

99-1248 

1887.0 

285.63 

503-4348 

201.7 

28.66 

55.9-430.5 

&concentrations of six monoterpenes (tricyclene, a-pinene, camphene, 

P-pinene, myrcene, menthene-1) and one oxygenated monoterpene (bornyl 

acetate), the principal components of the oleoresin of these trees, are 

presented. Additional monoterpenes (a-phellandrene, ~-·3-carene, t-limonene, 

terpinolene) and oxygenated monoterpenes (cis-P-terpineol, t-borneol) that 

were minor components of the oleoresin were included when calculating terpene 

totals. 

bcurrent-year needles collected in late June 1988, when western spruce 

budworms were in the late-instar feeding period. 

cProbability level for a paired t-test comparing foliar chemistry for 

resistant and susceptible Douglas-fir trees, df - 11. 

CONCLUSIONS 

Foliar analyses of 1988 new growth revealed that defoliation susceptible Douglas-fir had lower 

levels of N and sugars in their foliage than nearby defoliation resistant trees. Susceptible trees, 

moreover, had higher mineral/N ratios for P, K, Ca, Mg, and Zn. These field data are consistent with 

predictions made from laboratory diet experiments that high mineral/N ratios favor spruce budworm 

population growth. In other words, the susceptible trees had sugar concentrations and mineral/N ratios 

closer to the optimal levels for the spruce budworm than did the resistant trees. The results, 

therefore, support the hypothesis that variations in levels of foliar nutrients among individual trees may 

be an important mechanism in Douglas-fir resistance to C. occidentalis damage. Resistant trees may 

suffer low defoliation because they provide a food source that is poorly matched to the budworm's 

nutritional requirements with respect to concentrations of sugars and balances of key minerals to N. 

129 
A potential caveat must be attached to these results, however. Although there were detectable 

differences in sugar concentrations and mineral/N ratios between apparently resistant and susceptible 

trees, neither group was close to the optimal levels estimated from diet experiments. This implies that 

host plants rarely provide a food resource which closely matches the budworm's most favorable 

conditions for growth and reproduction. 

Terpenoid compounds did not appear to be related to resistance to budworm attack because 

there were no detectable differences between monoterpene concentrations in putatively resistant and 

susceptible trees. This result was somewhat surprising because terpene compounds have frequently 

been implicated as important determinants of western spruce budworm performance (Redak 1982, Cates 

et al. 1983a, 1983b, 1987, Perry and Pitman 1983, Redak and Cates 1984, Cates 1985, Shepherd 1985, 

Wagner and Tinus 1985, Cates and Redak 1986, 1988, Campbell 1987, Hermann 1987, Wulf and Cates 

1987, Wagner et al. 1989, 1990). However, the sample size was small (12 pairs of trees) and 

observations were highly variable, so the significance of the failure to detect differences may be open to 

question. Moreover, I only measured monoterpenes and sesquiterpenes, not larger terpenoids such as 

resin acids. 

Several possible alternatives may explain why foliar nutrients were different between susceptible 

and resistant Douglas-fir trees. First, the susceptible trees may truly have inherently different nutrient 

levels owing to their genetic make-up. Second, the foliar chemistry of resistant versus susceptible trees 

may have been induced by the dissimilar defoliation histories, which are a consequence of some 

unmeasured tree properties (Piene 1980). If this is the case, it implies that budworm defoliation has a 

positive feedback for subsequent generations, as in the "resource regulation hypothesis" proposed by 

Craig et al. (1986). Third, it is possible that resistant trees support budworm populations equal to 

those supported by susceptible trees, but the larvae consume less of the annual foliage increment 

because a) the food contains more N and b) the trees produce more foliage. In other words, resistant 

trees suffer substantially less defoliation. A fourth plausible explanation involves phenology of 

budbreak. Resistant trees may break bud later than susceptible trees and consequently be consistently 

asynchronous with budworm emergence. I am investigating these alternative explanations in greenhouse 

bioassay experiments with replicated isogenic lines of resistant and susceptible trees. 

SUMMARY 

The western spruce budworm (Choristoneura occidentalis) and Douglas-fir (Pseudotsuga menziesii) 

provide a good model system by which to test the hypothesis that variation in host plant nutritional 

quality is a mechanism for plant resistance to herbivore attack. In this study I compared levels of 

several nutrients (nitrogen, sugars, phosphorus, potassium, calcium, magnesium, and zinc) and terpenes 

in foliage of Douglas-fir trees that were phenotypically resistant and susceptible to western spruce 

budworm defoliation. The field results were compared with the results of artificial diet experiments 

designed to determine the budworm's response curves to individual nutrients. 

This first year's (1988) field data revealed that susceptible Douglas-fir trees had lower levels of 

foliar N and sugars than resistant trees, agreeing with predictions made from laboratory diet studies. 

Moreover, the susceptible trees had mineral/N ratios (for P, K, Ca, and Zn) which were closer to the 

optimal levels established in artificial diet studies. There were no detectable differences in 

monoterpenes between susceptible and resistant Douglas-fir trees. 

130 
ACKNOWLEDGMENTS 

I would like to thank R.M. King, R. W. Tin us, and M.R. Wagner for their comments on the 

manuscript. I am grateful to J.K. Itami for assistance with the field work and to R. Foust and 

T. Huntsberger for conducting the chemical analyses. My western spruce budworm colony was started 

with egg masses obtained from the Insect Production Unit of the Forest Pest Management Institute, 

Forestry Canada, in Sault Ste. Marie, Ontario. 

LITERATURE CITED 

BROOKES, M.H., CAMPBELL, R.W., COLBERT, J.J., MITCHELL, R.G., and STARK, R.W., eds. 

1987. Western spruce budworm. U.S. Dep. Agric. For. Serv. Tech. Bull. 1694. 198 p. 

CAMPBELL, R.W. 1987. Population dynamics, p. 71-88. In Brookes, M.H., Campbell, R.W., Colbert, 

J.J., Mitchell, R.G., and Stark, R. W., eds. Western spruce budworm. U.S. Dep. Agric. For. Serv. 

Tech. Bull. 1694. 198 p. 

CATES, R.G. 1985. The effect of chemical defenses, nutrition, needle phenology, and physical 

parameters of Douglas-fir on western spruce budworm success, p. 128-129. In Sanders, C.J., 

Stark, R.W., Mullins, E.J., and Murphy, J., eds. Recent advances in spruce budworms research. 

Minist. Supply Serv. Can. Cat. No. Fo18-5/1984. 527 p. 

CATES, R.G. and REDAK, R.A 1986. Between-year population variation in resistance of Douglas-fir 

to the western spruce budworm, p. 106-115. In Green, M.B. and Hedin, P.A, eds. Natural 

Resistance of Plants to Pests: Roles of Allelochemicals. American Chemical Society, Washington, 

D.C. 243 p. 

CATES, R.G. and REDAK, R.A 1988. Variation in the terpene chemistry of Douglas-fir and its 

relationship to western spruce budworm success, p. 317-344. In Spencer, K.C., ed. Chemical 

Mediation of Coevolution. Academic Press, New York. 609 p. 

CATES, R.G., REDAK, R.A, and HENDERSON, C.B. 1983a. Patterns in defensive natural product 

chemistry: Douglas-fir and western spruce budworm, p. 3-19. In Hedin, P., ed. Plant Resistance 

to Insects. American Chemical Society, Washington, D.C. 375 p. 

CATES, R.G., REDAK, R.A, and HENDERSON, C.B. 1983b. Natural product defensive chemistry of 

Douglas-fir, western spruce budworm success, and forest management practices. Z ang. Entomol. 

96: 173-182. 

CATES, R.G., HENDERSON, C.B., and REDAK, R.A 1987. Responses of the western spruce 

budworm to varying levels of nitrogen and terpenes. Oecologia 73: 312-316. 

CLANCY, K.M. In press. A multiple-generation bioassay for investigating western spruce budworm 

(Lepidoptera: Tortricidae) nutritional ecology. Environ. En to mol. 

CLANCY, K.M., WAGNER, M.R., and TINUS, R.W. 1988a. Variations in nutrient levels as a defense: 

identifying key nutritional traits of host plants of the western spruce budworm, p. 203-213. In 

Mattson, W.J., l..evieux, J., and Bernard-Dagan, C., eds. Mechanisms of Woody Plant Defenses 

Against Insects: Search for Pattern. Springer-Verlag, New York. 416 p. 

CLANCY, K.M., WAGNER, M.R., and TINUS, R.W. 1988b. Variation in host foliage nutrient 

concentrations in relation to western spruce budworm herbivory. Can. J. For. Res. 18: 530-539. 

131 
COOK, J.L., HOUSEWEART, M.W., KULMAN, H.M., and THOMPSON, L.C. 1979. Foliar mineral 

differences related to sawfly defoliation of white spruce. Environ. Entomol. 7: 780-781. 

CRAIG, T.P., PRICE, P.W., and ITAMI, J.K. 1986. Resource regulation by a stem-galling sawfly on the 

arroyo willow. Ecology 67: 419-425. 

DENNO, R.F. and McCLURE, M.S., eds. 1983. Variable Plants and Herbivores in Natural and 

Managed Systems. Academic Press, New York. 717 p. 

HARVEY, G.T. 1974. Nutritional studies of eastern spruce budworm (Lepidoptera: Tortricidae) 

1. Soluble sugars. Can. Entomol. 106: 353-365. 

HERMANN, R.K. 1987. Description of host species, p. 43-56. In Brookes, M.H., Campbell, R.W., 

Colbert, J.J., Mitchell, R.G., and Stark, R.W., eds. Western spruce budworm. U.S. Dep. Agric. 

For. Serv. Tech. Bull. 1694. 198 p. 

KEMP, W.P. and MOODY, U.L. 1984. Relationships between regional soils and foliage characteristics 

and western spruce budworm (Lepidoptera: Tortricidae) outbreak frequency. Environ. Entomol. 

13: 1291-1297. 

MATTSON, W.P. and SCRffiER, J.M. 1987. Nutritional ecology of insect folivores of woody plants: 

water, nitrogen, fiber, and mineral considerations, p. 105-146. In Slansky, F. and Rodriguez, J., 

eds. Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates. John Wiley & 

Sons, New York. 1016 p. 

MATTSON, W.J., LORIMER, N., and LEARY, R.A 1982. Role of plant variability (trait vector 

dynamics and diversity) in plant/herbivore interactions, p. 295-303. In Heybroek, H.M., Stephan, 

B.R., and Von Weissenberg, K., eds. Resistance to Diseases and Pests in Forest Trees. Pudoc, 

Wageningen, Netherlands. 503 p. 

MATTSON, W.J., LEVIEUX, J., and BERNARD-DAGAN, C., eds. 1988. Mechanisms of Woody Plant 

Defenses Against Insects: Search for Pattern. Springer-Verlag, New York. 416 p. 

PERRY, D.A and PITMAN, G.B. 1983. Genetic and environmental influences in host resistance to 

herbivory: Douglas-fir and the western spruce budworm. J. Appl. Entomol. 96: 217-228. 

PlENE, H. 1980. Effects of insect defoliation on growth and foliar nutrients of young balsam fir. 

For. Sci. 26: 665-673. 

REDAK, R.A 1982. A determination of the resistance-susceptibility characteristics in Douglas-fir to the 

western spruce budworm. M.S. thesis. Univ. New Mexico, Albuquerque, NM. 85 p. 

REDAK, R.A and CATES, R.G. 1984. Douglas-fir (Pseudotsuga menziesii)-spruce budworm 

(Choristoneura occidentalis) interactions: the effect of nutrition, chemical defenses, tissue 

phenology, and tree physical parameters on budworm success. Oecologia 62: 61-67. 

SHEPHERD, R.F. 1985. A theory on the effects of diverse host-climatic environments in British 

Columbia on the dynamics of western spruce budworm, p. 60-70. In Sanders, C.J., Stark, R.W., 

Mullins, E.J., and Murphy, J., eds. Recent advances in spruce budworms research. Minist. Supply 

Serv. Can. Cat. No. Fo18-5/1984. 527 p. 

132 
WAGNER, M.R. and TINUS, R. W. 1985. Mechanisms of tree resistance to spruce budworms--is there 

a terpene connection? p. 121-123. In Sanders, C.J., Stark, R.W., Mullins, E.J., and Murphy, J., 

eds. Recent advances in spruce budworms research. Minist. Supply Serv. Can. Cat. No. Fo18-

5/1984. 527 p. 

WAGNER, M.R., CLANCY, K.M., and KIRKBRIDE, D.M. 1987. Predicting number of oocytes in 

adult western spruce budworm, Choristoneura occidentalis (Lepidoptera: Tortricidae ). Environ. 

Entomol. 16: 551-555. 

WAGNER, M.R., CLANCY, K.M., and TINUS, R.W. 1989. Maturational variation in needle essential 

oils from Pseudotsuga menziesi~ Abies concolor and Picea engelmanii. Phytochemistry 28: 765-770. 

WAGNER, M.R., CLANCY, K.M., and TINUS, R.W. 1990. Seasonal patterns in the allelochemicals of 

three coniferous hosts of the western spruce budworm, Choristoneura occidentalis. Biochem. Syst. 

Ecol. 18: 215-220. 

WULF, N.W. and CATES, R.G. 1987. Site and stand characteristics, p. 89-115. In Brookes, M.H., 

Campbell, R.W., Colbert, J.J., Mitchell, R.G., and Stark, R.W., eds. Western spruce budworm. 

U.S. Dep. Agric. For. Serv. Tech. Bull. 1694. 198 p. 

133 
PA'I'I'ERNS OF NUTRIENT UTILIZATION 

IN THE NEEDLE-FEEDING GUILD 

THOMAS SECHER JENSEN 

Zoological Laboratory 

Institute of Zoology and Zoophysiology 

University of Aarhus, DK-8000 Aarhus, Denmark 

INTRODUCTION 

It is well known that large differences in performance parameters such as growth rate, survival 

rate, or fecundity rate are found between various insect guilds, e.g. root feeders and sapsuckers (Siansk.y 

and Rodriguez 1987, Slansk.y and Scriber 1985). Within guilds and even within a given host plant, the 

variability of the plant material may also result in considerable differences in the performance 

parameters of insect larvae feeding on the plant (Whitham 1983, Jensen 1988). 

Under constant laboratory conditions, variability in performance depends primarily on the 

nutrient and secondary compound content of the host plant material. Positive correlations between 

performance parameters and the carbohydrate, amino acid, or total nitrogen content can be found, 

while negative correlations have often been made between performance and the presence of phenolics, 

tannins, or alkaloids. 

With a limited number of insect species such correlative analyses might be tested by using 

artificial diet studies. In such studies, however, it is extremely difficult to mimic the true composition 

of the various chemicals in the plant tissue. Another method is to study the fate of various 

biochemicals when ingested by a certain insect. 

In the present investigation, the content of various biochemicals in the needles of conifers (Pinus 

and Picea species) was compared with the content of the same compounds in larval feces for a number 

of insect species within the needle-feeding guild These species comprise conifer specialists within the 

Lepidoptera (Bupalus pinarius, Dendrolimus pini, Panolis flammea) and Hymenoptera (Diprion pini, 

Neodiprion sertifer, Pristiphora abietina, Gilpinia hercyniae, Pachynematus scutellatus, Cephalcia abietina) 

as well as the generalists, mainly Lepidoptera (Orgya antiqua, Lymantria monacha), known to use host 

plants other than the conifers. 

EXPERIMENTAL METHODS 

All insects were reared under standardized conditions, at 200C and with 18 hr daylight, on whole 

branches cut from 40 to 60-year-old spruce and pine trees. First instar larvae were kept in groups, 

later instars singly. Most individuals were wild-captured or first generation laboratory-reared with the 

exception of Diprion pini, which came from the stock maintained at the University of Turku, Finland. 

BARANCHIKOV, Y.N., MATfSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

134 
Samples of needles were taken at the start and in the middle of the experimental period, and 

larval feces samples were collected 2 to 3 days after the needle samples were taken. Needles and feces 

were freeze-dried, ground, and stored in a desiccator in the dark at room temperature. 

Polar compounds were extracted three times with methanol, 2 ml for 15 min at 65°C, each time 

with subsequent centrifugation, 5 min 2800 U/min at room temperature. The methanol extract was 

derivatized by oxime formation followed by silylation and applied to a gas chromatographic column 

(2m x 4mm) packed with SE52 on Chromosorb G. The internal standard method was used to 

determine the quantities derived from the chromatograms. 

The total nitrogen content of the freeze-dried material was determined by means of the modified 

micro-Kjeldahl method. 

RESULTS 

Total Nitrogen 

As expected, the total nitrogen content in conifer needles differs between old and young needles, 

highest values (ca. 4 percent dwt) being found in the newly flushed needles and decreasing as the 

needles grow old. Even at the start of the growing season, old needles have a very low ( < 1 percent 

dwt) nitrogen content. 

Fig. 1 shows the concentration of nitrogen in spruce and pine needles compared with the 

concentration of nitrogen in the feces of several insect species. The consensus for all species and all 

types of food is that nitrogen utilization is low. The concentration of nitrogen in the feces is only 

slightly lower than that in the needles. Even in cases where the food has a content of about 

1 percent, the concentration in the feces is close to the value in the needle. When the metabolic 

quotient is taken into account, the general utilization of nitrogen in these species is in the order of 

45 to 55 percent. 

Carbohydrates 

In the present investigation, the concentrations of fructose, alpha- and beta-glucose, and sucrose 

were measured individually and the total amount of hexose-equivalents calculated as: 

Chex = Fru + Glu + 2(Suc) 

In pines few differences in carbohydrate concentrations were found between old and young 

needles, whereas among spruce somewhat higher concentrations were found in old than in the younger 

needles. 

Fig. 2 shows the level of carbohydrates in the feces of all insect species investigated. The 

consensus for all species on all food resources is utilization is very high, 95 to 100 percent. Even 

when carbohydrate concentrations are very elevated, the utilization is almost complete. Carbohydrate 

values from insect consumption of male flowers are not included in the figure, but male flowers can 

have carbohydrate concentrations of 600 to 1,300 nmoles/g dwt, and in such cases the utilization is still 

95 to 100 percent. 

135 
~ 

~ 

NEW 

NITROGEN (0/o dwt) 

II Foliage 

SPRUCE NEEDLES 

OLD 

lyman tria 

Pachynematus 

0 Frass 

NEW 

5 Jlymantria 

4 

a 

2 

4 

a 

2 

Diprion 

Neodiprion 

o------~ 

PINE NEEDLES 

OLD 

Lyman tria 

th Diprion 

Neodiprion 

Figure 1. Concentrations of total nitrogen in new and old needles of spruce and pine, and in frass of 

insect herbivores. 
,..... 

(,;.) 

-l 

CARBOHYDRATES (nmoles/g dwt) 

II Foliage 0 Frass 

SPRUCE NEEDLES PINE NEEDLES 

NEW OLD NEW OLD 

Lyman tria 4001 Lymantria ... 1 Lymantria 4001 Lymantria 

Orgya Cephalcia 

Pristiphora Neodiprion 

Figure 2. Concentrations of carbohydrates (hexose-equivalents of sucrose, fructose, and glucose) in new and 

old needles of spruce and pine, and in frass of insect herbivores. 
Cyclites 

Fig. 3 shows the concentrations of the conifer-specific cyclite (sugar alcohol), pinitol. Pinitol 

occurs in rather high concentrations, highest in the new needles. Male flowers also contain high 

amounts of pinitol. In most insect species there seems to be an almost complete utilization of this 

compound, although Lymantria monacha has a somewhat lower assimilation leveVrate when eating old 

needles. When the concentration of pinitol in the food is very high, however, utilization seems to 

decrease. 

The other cyclite, inositol, occurs in much lower concentrations (7 to 25 nmoles/g dwt) in the 

needles and in the male flowers. At low concentrations, all inositol is utilized, but at higher 

concentrations in the food, inositol can occur in concentrations of up to 17 nmoles/g dwt in 

L. monacha feces. 

Phenolic Acids 

Quinic acid is the low-molecular compound in conifer needles found in probably the most 

variable concentrations, ranging from 35 to 1,000 nmoles/g dwt. The high concentrations are found in 

newly flushed needles and in the male flowers of spruce and the lower concentrations in old pine 

needles. 

Fig. 4 shows that the pattern of utilization of quinic acid is highly variable, depending on the 

insect/host plant system. The generalist L. monacha seems to tolerate this compound, quinic acid 

being present in the feces in concentrations equal to or even higher than in the needles. Taking the 

metabolic quotient into account, one may infer low or zero utilization. 

The same pattern is found in the other generalist lepidopteran, Orgya antiqua, feeding on new 

spruce needles. The specialist pine lepidopterans, Bupalus pinarius and Dendrolimus pini, seem to 

follow the same pattern as well, and with them higher concentrations in the feces than in the old pine 

needles clearly indicate that quinic acid passes through the intestine unaltered. 

In striking contrast, the specialist sawflies seem to utilize at least a part of the quinic acid when 

reared on their proper host. When Diprion pini and Neodiprion sertifer feed on old pine needles, 

concentrations of quinic acid in the feces are quite low. However, when these species are forced to 

feed on new needles with a higher content of quinic acid, the concentrations in the feces are higher, 

but still below the value in the needles. 

The spruce specialist sawflies seem to follow this pattern. Although given higher concentrations 

of quinic acid in spruce needles, higher levels are also found in the feces, utilization seems to be 

similar. 

Shikimic acid also shows a variable pattern between plant species and plant parts, highest values 

being found in old spruce needles and in Pinus contorta and lowest values in new spruce needles and 

male pine flowers (Fig. 5). 

138 
...... 

(j.) 

\0 

CYCLITES (nmoles/g dwt) 

II Foliage 0 Frass 

SPRUCE NEEDLES PINE NEEDLES 

NEW OLD NEW OLD 

Lyman tria Lymantria Lyman tria Lyman tria 

100 

Orgy a 2001 Cephalcia Diprion 

100 

0 • 

Pristiphora 2001 Pachynematus 2001 Neodiprion 

o----' 

·:~ L 

Figure 3. Concentrations of the cyclite, pinitol, in conifer needles and in herbivore frass. 
QUINIC ACID (nmoles/g dwt) 

II Foliage 0 Frass 

SPRUCE NEEDLES PINE NEEDLES 

NEW OLD NEW OLD 

Lyman tria Lyman tria Lymantria 1 Lymantria 

aoot 1100 800 8CID 

- 600 600 100 

400 400 400 

2~1 I I 200 200 200 

0 

____, " 0 

1-" 

+:-. 

0 Cephal cia Diprion • Diprion 

800 800 800 

800 800 100 

400 400 I 400 

""' 200 

200 

0 

Pachynematus Neodiprion Neodiprion 

100 

1100 

100 

1100 

..., 

400 

200 

200 

o' ----..., 0,~----~-.---------

Figure 4. Concentrations of quinic acid in conifer needles and in herbivore frass. 
..... 

~ 

..... 

NEW 

Lyman tria 

Orgya 

0"----

Pristiphora 

SHIKIMIC ACID (nmoles/g dwt) 

II Foliage 0 Frass 

SPRUCE NEEDLES PINE NEEDLES 

OLD NEW OLD 

lyman tria Lyman tria 

Diprion 

Pachynematus .. och Neodiprion 

300 

200 

'IOOi I 

0 --, 

Figure 5. Concentrations of shikimic acid in conifer needles and in herbivore frass. 
Likewise the variability of shikimic acid utilization by needle-feeding insects is considerable. The 

concentration of shikimic acid in the feces of L. monacha is often higher than in the food, indicating 

that the compound passes through the intestine unmetabolized. The same holds for another generalist 

lepidopteran, Orgya antiqua, and the pine specialist lepidopterans, Bupalus pinarius, Dendrolimus pinus, 

and Panolis jlammea. 

In contrast, all specialist sawflies, irrespective of host plant and plant part, show fairly high 

utilization of shikimic acid. 

DISCUSSION 

The results of our analyses clearly show that in all conifer insect species investigated, the 

utilization of carbohydrates (fructose, glucose, and sucrose) was almost 100 percent. This strongly 

suggests that demand for carbohydrates in the concentrations found in conifer needles is high among 

needle-feeding herbivores. It also suggests that carbohydrates may be a limiting factor in certain 

performance parameters for those insect species consuming the most carbohydrate-poor diet. 

Studies of insect performance in relation to carbohydrate concentrations have so far given rather 

different results, however. Positive correlations have been found in Gilpinia hercyniae/Picea abies 

(Schopf 1986, Jensen 1988), Sphinx pinastri/Pinus silvestris (Otto 1970), and Choristoneura 

fumiferana/Picea glauca (Harvey 1974, McLaughlin 1986). Nonsignificant correlations have been 

described in C. fumiferana/Abies balsamea (Shaw et al. 1978). 

Although cyclites are carbohydrates, they seem to differ from them in having a somewhat lower 

utilization rate. In particular, pinitol, when highly concentrated in the needles, is sometimes found in 

high concentrations in the feces as well. In any case, the cyclites add to the general pool of energy 

available to the herbivores. 

Nitrogen is one of the compounds most often related to insect performance (Mattson 1980, 

Mattson and Scriber 1987). Thus it is interesting to note that in the present investigation nitrogen was 

found to be utilized only to a limited degree by the foliage-feeding herbivores. This may be due to the 

indigestible nature of the N compounds or to large concentrations of digestibility-reducing compounds, 

e.g. tannins or resins, which can lower the bioavailability of the proteins in the needles (Rhoades 

1983). As nitrogen utilization was low and the concentration of nitrogen high in the feces of species 

eating newly flushed needles, however, concentrations of digestibility-reducing compounds should also 

be high in these new needles. This is not consistent with general theory and not supported by 

available data. By way of explanation, one could argue that the results obtained here are derived 

mainly from later instar larvae and that newly hatched larvae would have a greater demand for and 

therefore a higher utilization of nitrogen. 

The highly variable utilization of quinic acid and shikimic acid may be interpreted in relation to 

their potential role as secondary compounds. Utilization of these acids is rather low among generalist 

and specialist lepidopterans, and the part of the compounds excreted. Accordingly, these insect species 

do not receive the potential carbon-energy from the compounds in question, but have, on the other 

hand, developed a tolerance for acidity and merely excrete the acids. 

The specialist sawflies, unlike the lepidopterans, seem to metabolize part of the acids and hence 

obtain carbon-energy, probably by means of microbial activity in the mid-gut (Schopf 1986), but this 

adaptation often limits them to a very specific host-range, some of the species being unable to tolerate 

needles of a certain age class even from their favorite host. Gilpinia hercyniae often dies on immature 

spruce needles (Jensen 1988). Neodiprion sertifer and Diprion pini have a high preference for old, pine 

needles, though if forced to eat new needles, they are able to survive. 

142 
CONCLUSIONS 

Results of the present investigation seem to indicate that the main differences in utilization of 

nutrients and secondary compounds within the needle-feeding guild exist along taxonomical lines 

(Hymenoptera-Lepidoptera) rather than generalist-specialist lines. Both orders have developed a high 

capacity of carbohydrate utilization and perhaps a lower capacity of nitrogen utilization. Both specialist 

and generalist lepidopterans seem unable to metabolize, but able to tolerate certain secondary 

compounds, whereas hymenopterans, all specialists, utilize these compounds to varying degrees. 

SUMMARY 

The nutrient content and the content of certain low molecular secondary compounds of conifer 

needles and flowers from Picea and Pinus species were quantified by means of gas chromatography and 

micro-Kjeldahl analysis. The same compounds were also quantified in the feces of conifer insects 

(Lepidoptera and Hymenoptera) within the herbivore guild. Carbohydrates and cyclites in the needles 

and in the flowers were almost totally utilized by these insect species, whereas only 45 to 55 percent of 

the total nitrogen content was utilized. Among specialist and generalist lepidopterans, secondary 

compounds such as shikimic acid and quinic acid were utilized only to a very low degree, whereas 

among specialist hymenopterans (sawfly species), utilization of these compounds was high. 

LITERATURE CITED 

HARVEY, G.T. 1974. Nutritional studies of eastern spruce budworm. I. Soluble sugars. Can. Entomol. 

106: 353-365. 

JENSEN, T.S. 1988. Variability of Norway spruce (Picea abies) needles; performance of spruce sawflies 

(Gilpinia hercyniae). Oecologia 77: 313-320. 

MATTSON, W.J. 1980. Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst. 

11: 119-161. 

MATTSON, W.J. and SCRIBER, J.M. 1987. Nutritional ecology of insect folivores of woody plants: 

nitrogen, water, fiber, and mineral considerations, pp. 105-146. In Slansky, F. and Rodriguez, 

J.G., eds. Nutritional Ecology of Insects, Mites, Spiders, and Related Invertebrates. John Wiley 

& Sons, New York. 

McLAUGHLIN, B.M. 1986. Performance of the spruce budworm (Choristoneura fumiferana) in relation 

to dietary and foliar levels of sugar and nitrogen, p. 1-86. Unpubl. thesis. Michigan State Univ. 

OTTO, D. 1970. Zur Bedeutung des Zuckergehaltes der Nahrung fiir die Entwicklung nadelfressender 

Kieferninsekten. Arch. Forstwes. 19: 135-150. 

RHOADES, D. 1983. Herbivore population dynamics and plant chemistry. In Denno, R.F. and 

McClure, M.S., eds. Variable plants and herbivores in natural and managed systems. 

SCHOPF, R. 1986. The effect of secondary needle compounds on the development of phytophagous 

insects. For. Ecol. Manage. 15: 55-64. 

SHAW, G.G., LITTLE, C.H.A, and DURSAN, D.J. 1978. Effect of fertilisation of balsam fir trees on 

spruce budworm nutrition and development. Can. J. For. Res. 8: 364-374. f 

143 
SLANSKY, F. and RODRIGUEZ, J.G. (eds.). Nutritional ecology of insects, mites, spiders, and related 

invertebrates. John Wiley & Sons, New York. 1016 p. 

SLANSKY, F. and SCRIBER, J.M 1985. Food consumption and utilization, p. 87-16. In Kerkut, G.A 

and Gilbert, LI., eds. vol 4. Comprehensive insect physiology, biochemistry and pharmacology. 

WHITHAM, T.G. 1983. Host manipulation of parasites: within-plant variation as a defense against 

rapidly evolving pests, p. 15-41. In Denno, R.F. and McClure, M.S., eds. Variable plants and 

herbivores in natural and managed systems. 

144 
THE FOLIVORE GUILD ON LARCH (LARIX DECIDUA) 

IN THE ALPS 

W. BALTENSWEILER 

Institute of Plant Sciences, Division of Phytomedicine 

ETH-Zentrum/CLS 

CH 8092 Zurich, Switzerland 

In memoriam Christian Auer 

INTRODUCfiON 

The term "guild" describes a group of organisms that exploit the same class of resources in a 

similar manner (Root 1967, Mattson et al. 1988). This study focuses on six members of the folivore 

guild of subalpine larch, Larix decidua, in Switzerland--five lepidopterans and one hymenopteran. From 

1949 to 1979, Auer (1977) sampled populations of the larch bud moth, Zeiraphera diniana L., and at 

the same time collected associated larvae. I have analyzed these 30 years of insect sample data for the 

six different species and now offer it to the scientific literature. In spite of some methodological 

shortcomings, the data have tremendous value because of their historical import. There are precious 

few long-te,-m data sets of this kind. 

The spectacular population cycles of the larch bud moth (LBM) and the ensuing periodic severe 

defoliations of the subalpine larch forests have provided an interesting opportunity to analyze possible 

interspecific competition among members of the larch folivore guild owing to varying degrees of 

depletion of their common food source. The impact of defoliation on each member of the guild is 

evaluated by comparing trends (immediate and delayed) in the population index of each with the larch 

bud moth (LBM) cycle. 

By analogy to what happens to the LBM, "immediate impact" is understood as increased larval 

mortality and reduced fecundity due to loss of shelter and starvation, whereas "delayed impact" results 

from the "induced response" which is mediated by the lower food quality in years subsequent to 

defoliation and results in drastically increased mortality of the small larvae for several succeeding 

generations. I used Chi-square analysis to compare the trends in fluctuation patterns of the guild 

members with the LBM. I examine the hypothesis that interspecific competition driven by the LBM 

contributes to the quantitative structuring of the guild. 

EXPERIMENTAL METHODS 

Biology and Phenology of Guild Members 

Although there are many insects associated with the large larval instars of the LBM, only the six 

most frequent phytophagous species are considered (Fig. 1 ). 

BARANCHIKOV, Y.N., MA1TSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

145 
1) Tortricidae 

a) Exapate duratella Heyd. is polyphagous on mountain ash (Sorbus aucuparia), shrubs 

(Vaccinium, Rhododendron, and Cotoneaster), or herbs (Thalictrum) growing underneath 

larch (Thomann 1947). It occurs throughout the alpine region and overwinters in the 

egg stage. Hatching occurs somewhat later than the LBM. It has five larval instars 

which construct fascicles similar to those of the LBM. Rather agile when disturbed, 

they descend on silken threads to lower branches or to the ground. If not disturbed, 

E. duratella pupates on larch. The species is sexually dimorphic: males are winged 

and white; females are wingless and dark gray. Females are very cold-hardy, surviving 

temperatures as low as -1SOC, and are active at air temperatures as low as soc 

(Baltensweiler 1961). 

b) Ptycholomoides aeriferana H.-Schaeff. is oligophagous on Acer platanoides, Larix, and 

pine (Raigorodskaya 1963). Palearctic in distribution, it is found from Europe to 

Japan. This species hatches from the egg in fall, molts to the second instar without 

feeding, and overwinters in diapause. It starts to feed in the spring, simultaneous with 

the LBM. After the fifth larval instar, pupation takes place between the needles. The 

female attaches her eggs to the needles by means of an adhesive substance. Highest 

densities usually occur at altitudes below 1700 m. 

c) Spilonota laricana Hein. is monophagous on larch and palearctic in distribution (Bovey 

1978). The eggs are deposited on needles in June to August, depending on altitude. 

The first instar larvae hatch after 2 weeks and overwinter as second instar larvae in a 

hibemaculum. Emergence takes place during needle growth of larch. The larvae 

construct a fascicle similar to that of the LBM. Pupation occurs between needles and 

the moths emerge after 2 to 3 weeks. Highest densities usually occur at altitudes 

below 1700 m. 

2) Geometridae 

Oporinia (Epirrita) autumnata Bkh. is polyphagous, living on birch, larch, fir, and spruce. 

Extensive outbreaks occur on birch in Scandinavia (Tenow 1972). The species being 

univoltine, eggs are deposited singly on branches, where they overwinter. Hatching occurs in 

early spring. The five larval instars live openly along the branch axis and feed on needles 

without spinning a fascicle. Thus the larvae are very easily dislodged when the branch 

samples are collected if precautions are not taken. Losses of 30 percent and 53 percent 

were observed when the branch samples were thrown to the ground from the lower and 

middle to upper crown levels respectively (Bidaud 1970). Pupation occurs on the ground. 

The moths are not very good flyers. 

3) Gelechidae 

Teleia saltuum Z is oligophagous and palearctic in distribution. Its biology is not very well 

known, but the insect seems to occur primarily at low altitudes. It is a biennial species, 

overwintering both as L2- and LS-larvae. Eggs are deposited on needles. 

146 
Ill IV v VI VII V111 IX X XI XII 

Larix decidua 

Zeiraphera diniana / / eggs in post-diapause ggs in diapause 

Exapate duratella eggs in quiescence •·L1,5 p A /eggs 

Oporinia autumnata eggs in diapause L1-5 eggs in diapause 

Pt. aeriferana L2 in diapause L2 in diapause 

Spilonota laricana L3 in quiescence L3 in quiescence 

releia sa/tuum L, in quiescence 4 in quiescence 

~ in quiescence Ls in quiescence 

Pristiphora lanCis eggs in posl-diapause eo nymph 

Figure 1. Phenology and biology of the folivore guild on larch (Larix decidua 

Mill.) in the European Alps. 

4) Tenthredinidae 

Pristiphora laricis Htg. is monophagous and palearctic in its distribution. At lower altitudes 

two generations occur per year; above 1700 m only a partial second generation is observed. 

Overwintering as an eonymph in a cocoon, it transforms to a pronymph in January (Lovis 

1975), and the adults emerge toward the end of May and beginning of June. Eggs of the 

first generation are laid on the growing needles and hatch after 10 days at 16°C or 21 days 

at 100C. 

Larval Population Sample 

The sampling methodology for the LBM and its associated guild members (Killin and Auer 

1954, Auer 1961) relies on a sampling scheme stratified according to topography (altitude and 

exposure) and host tree density per unit area in the subalpine forest, e.g. Larici-pinetum-cembrae 

(Ellenberg and Klotzli 1972). The proper sample provides a basic population estimate for the larval 

stage of each generation on a weight basis, i.e. number of larvae per kg of larch twigs with foliage. It 

is comprised of three branches cut at three levels within the crown of the tree. The samples are taken 

when the LBM is in its fourth or fifth instar. This coincides phenologically with the time at which the 

larch needles cease to grow. 

Five outbreak areas along the alpine arch, covering 2120 to 6280 ha of montane and subalpine 

forests, were sampled between 1949 and 1976 with 100 to 500 sample trees for various periods (Auer 

1977): 

1) the region of the Brian~onnais in the western Alps (Department Hautes Alpes, France) 

2) the Goms in the Upper Rhone River Valley (Kanton Wallis, Switzerland) 

3) the Oberengadin (Kanton Graubunden, Switzerland) 

4) the Valle Aurina (Provincia Autonoma di Bolzano-Alto Adige, Italy) 

5) the Lungau (Land Salzburg, Austria). 

147 
Evaluation of the Defoliation Impact 

on the Guild Members 

Two negative effects of defoliation on the fluctuations of the guild members are conceivable. 

1) An immediate impact. Assuming that the destruction and depletion of the common food 

resource in the current generation t induces immediate larval mortality due to malnutrition 

or lack of shelter and reduces, therefore, the egg potential of the following generation, the 

immediate impact is a lower larval density in generation t + 1: 

(If Density LBMt > 100 larvae/kg: Density xt+ 1 < Density xt1· 

Pristiphora laricis, whose first generation larval period coincides exactly with the large larval 

stages of the LBM, might suffer heavy mortality in the same generation t, and therefore the 

immediate impact is defined by (Density Plt < Density Pit -11· 

2) A delayed impact. Defoliation of the larch lowers the long-term nutritional quality of the 

larch needles in subsequent generations, a condition which may relax only over the course of 

several years (Baltensweiler 1984, Baltensweiler and Fischlin 1988). This impact is defined 

as follows: 

(If Density LBMt > 100 larvae/kg: Density xt+2 < Density xt+l; 

Density Plt+l < Density Plt1· 

The differences in density are evaluated as trends only, and the occurrence of cases is tested 

by Chi-square analysis. The error probabilities are given as percentages. 

RESULTS 

The densities for the LBM and its associated species on larch in five different subalpine regions 

are presented in Tables 1 through 7. The fluctuation pattern of the guild as a whole is remarkably 

similar at all five subalpine sites. In four to five generations, the LBM increases by five orders of 

magnitude and transgresses the defoliation threshold of 100 larvae/kg twigs at regular intervals of 8 to 

9 years (Baltensweiler et al. 1977). Conversely, the numbers of the other guild members vary with a 

moderate amplitude between 0.01 and 5 larvae/kg twigs, but without exhibiting any particular trend. 

This is somewhat surprising since one might have assumed that the severe and widespread defoliation 

by the LBM would synchronize the fluctuations of the other phytophagous species with each other. 

148 
Table 1. Zeiraphera diniana density (larvae/kg) 

Year Brian~onnais Goms Oberengadin Valle Aurina Lung au 

1952 4.174 

1953 68.797 

1954 331.760 

1955 126.541 

1956 21.280 

1957 2.246 

1958 0.049 0.085 

1959 0.090 0.080 

1960 4.422 0.458 0.371 0.040 

1961 48.303 1.774 1.638 0.140 0.090 

1962 361.879 10.902 22.878 2.420 0.560 

1963 53.440 151.132 248.817 39.260 8.760 

1964 70.770 175.215 184.272 180.460 107.870 

1965 0.475 3.235 3.116 21.880 234.576 

1966 0.024 0.013 0.020 0.280 38.540 

1967 0.041 0.025 0.002 0.020 0.290 

1968 0.335 0.025 0.059 0.050 0.040 

1969 2.152 0.180 0.197 0.150 0.183 

1970 10.114 1.495 1.068 0.752 0.707 

1971 81.913 10.338 10.569 3.810 3.170 

1972 245.787 76.355 173.932 8.330 29.820 

1973 1.371 78.225 249.612 4.255 36.060 

1974 0.396 8.075 176.050 4.029 118.450 

1975 0.258 0.190 4.749 4.740 18.380 

1976 0.618 0.050 0.014 0.441 3.760 

1977 3.600 0.008 0.118 0.830 

1978 36.144 0.600 0.056 0.068 0.240 

1979 209.531 1.616 0.204 0.130 0.170 

149 
Table 2. Exapate duratella density (larvae/kg) 

Year Brian~onnais Goms Oberengadin Valle Aurina Lung au 

1952 0.018 

1953 0.282 

1954 0.826 

1955 0.134 

1956 0.018 

1957 0.002 

1958 0.012 0.004 

1959 0.050 0.070 

1960 1.402 0.497 0.220 0.090 

1961 2.945 0.241 0.166 0.100 0.040 

1962 5.556 0.451 1.228 0.160 0.090 

1963 3.500 1.130 5.573 0.490 0.250 

1964 0.330 0.960 2.830 0.280 0.200 

1965 0.030 0.207 0.388 0.170 0.212 

1966 0.008 0.010 0.011 0.010 0.140 

1967 0.055 0.010 0.022 0.010 0.050 

1968 0.413 0.050 0.034 0.070 0.050 

1969 0.432 0.170 0.099 0.020 0.069 

1970 0.530 0.325 0.619 0.163 0.100 

1971 1.258 0.798 1.411 0.310 0.310 

1972 1.179 0.615 6.833 0.220 0.150 

1973 0.210 2.145 2.844 0.118 0.190 

1974 0.028 0.530 0.798 0.128 0.100 

1975 0.220 0.060 0.042 0.110 0.090 

1976 0.542 0.045 0.008 0.039 0.110 

1977 1.360 0.010 0.176 0.080 

1978 1.288 0.040 0.015 0.078 0.010 

1979 6.133 0.101 0.050 0.010 0.050 

150 
Table 3. Oporinia autumnata density (larvae/kg) 

Year Brian~onnais Goms Oberengadin Valle Aurina Lung au 

1952 0.287 

1953 0.669 

1954 0.994 

1956 0.202 

1957 0.106 

1958 0.134 

1958 0.531 0.361 

1959 0.668 0.838 

1960 1.074 1.047 0.707 0.960 

1961 0.780 0.670 0.417 0.310 0.530 

1962 0.414 3.284 2.185 0.930 0.850 

1963 0.560 6.320 2.354 1.260 0.900 

1964 0.600 10.388 0.850 0.980 1.650 

1965 0.530 2.530 0.286 0.40 1.151 

1966 0.412 0.328 0.124 0.330 0.610 

1967 2.950 0.450 0.248 0.490 0.420 

1968 4.883 1.445 0.888 1.385 0.580 

1969 2.472 2.205 1.063 2.730 0.752 

1970 0.225 1.795 0.788 1.693 1.153 

1971 0.255 1.581 1.047 1.360 1.360 

1972 0.168 1.085 0.912 0.290 1.370 

1973 0.196 0.990 0.572 0.216 0.440 

1974 0.458 3.035 0.508 0.676 1.040 

1975 0.740 1.060 0.128 0.880 0.570 

1976 0.570 0.550 0.361 0.667 0.590 

1977 3.760 0.229 2.197 0.590 

1978 18.394 1.590 0.696 1.255 0.690 

1979 5.449 0.909 0.240 0.485 0.240 

151 
Table 4. Ptycholomoides aeriferana density (larvae/kg) 

Year Brian~onnais Goms Oberengadin Valle Aurina Lung au 

1952 0.001 

1953 0.018 

1954 0.006 

1955 0.002 

1956 0.001 

1957 0.001 

1958 0.001 0.002 

1959 0.001 0.002 

1960 0.225 0.007 0.002 0.010 

1961 0.037 0.001 0.002 0.010 0.010 

1962 0.667 0.113 0.026 0.070 0.020 

1963 0.160 0.085 0.032 0 .. 250 0.010 

1964 0.090 0.093 0.016 0.210 0.560 

1965 0.010 0.010 0.016 0.110 0.101 

1966 0.004 0.003 0.002 0.060 0.160 

1967 0.005 0.005 0.002 0.010 0.030 

1968 0.065 0.005 0.002 0.095 0.020 

1969 0.221 0.010 0.007 0.115 0.064 

1970 0.040 0.085 0.007 0.118 0.127 

1971 0.240 0.061 0.053 0.310 0.310 

1972 0.026 0.050 0.019 0.070 0.070 

1973 0.019 0.220 0.012 0.029 0.110 

1974 0.028 0.055 0.006 0.098 0.020 

1975 0.001 0.010 0.002 0.070 0.140 

1976 0.092 0.040 0.002 0.069 0.110 

1977 0.150 0.002 0.088 0.080 

1978 0.356 0.040 0.002 0.010 0.050 

1979 0.327 0.010 0.002 0.010 0.010 

152 
Table 5. Spilonota laricana density (larvae/kg) 

Year Brian~onnais Goms Oberengadin Valle Aurina Lung au 

1952 0.031 

1953 0.065 

1954 0.125 

1955 0.103 

1956 0.017 

1957 0.009 

1958 0.142 0.026 

1959 0.150 0.022 

1960 0.451 0.593 0.043 0.070 

1961 0.404 0.084 0.027 0.070 0.010 

1962 0.273 0.255 0.039 0.060 0.007 

1963 0.400 0.220 0.043 0.190 0.270 

1964 0.180 0.113 0.138 0.220 0.110 

1965 0.265 0.397 0.174 0.430 0.889 

1966 0.092 0.065 0.041 0.120 0.550 

1967 0.486 0.160 0.029 0.110 0.250 

1968 1.644 0.175 0.086 0.160 0.220 

1969 0.085 0.295 0.091 0.145 0.173 

1970 0.115 0.275 0.035 0.118 0.060 

1971 0.828 0.121 0.070 0.450 0.450 

1972 0.124 0.060 0.101 0.200 0.470 

1973 0.201 0.110 0.151 0.157 0.160 

1974 0.134 0.210 0.136 0.382 0.810 

1975 0.150 0.040 0.155 0.270 0.290 

1976 0.127 0.105 0.084 0.539 0.290 

1977 0.230 0.049 0.127 0.100 

1978 0.182 0.130 0.022 0.088 0.110 

1979 0.163 0.061 0.030 0.019 0.030 

153 
Table 6. Teleia saltuum density (larvae/kg) 

Year Brianc;onnais Goms Oberengadin Valle Aurina Lung au 

1952 0.297 

1953 0.166 

1954 0.162 

1955 0.033 

1956 0.024 

1957 0.042 

1958 0.234 0.018 

1959 0.185 0.112 

1960 0.338 0.500 0.056 0.580 

1961 0.321 0.240 0.040 1.310 0.430 

1962 0.111 0.363 0.125 0.590 0.280 

1963 0.130 0.360 0.061 3.050 1.450 

1964 0.030 0.080 0.028 0.110 0.210 

1965 0.040 0.105 0.073 1.210 1.354 

1966 0.028 0.143 0.026 0.180 0.270 

1967 0.202 0.130 0.046 0.210 0.950 

1968 0.680 0.100 0.038 0.420 0.310 

1969 0.452 0.215 0.113 0.940 0.391 

1970 0.065 0.325 0.060 0.497 0.313 

1971 0.169 0.197 0.034 2.340 2.340 

1972 0.051 0.050 0.068 1.950 1.200 

1973 0.024 0.030 0.006 0.206 .0.230 

1974 0.013 0.060 0.010 2.274 1.140 

1975 0.040 0.010 0.013 0.410 0.190 

1976 0.077 0.010 0.008 0.559 0.970 

1977 0.080 0.006 0.608 0.670 

1978 0.058 0.040 0.007 0.225 0.850 

1979 0.041 0.020 0.220 0.010 0.220 

154 
Table 7. Pristiphora laricis density (larvae/kg) 

Year Brian~onnais Goms Oberengadin Valle Aurina Lung au 

1952 0.181 

1953 0.198 

1954 0.352 

1955 0.084 

1956 0.225 

1957 0.887 

1958 1.901 2.587 

1959 1.345 2.657 

1960 0.525 2.500 1.986 4.500 

1961 0.514 0.394 0.949 1.920 2.340 

1962 0.929 1.402 2.284 1.880 5.010 

1963 0.360 0.400 0.939 1.450 3.730 

1964 0.730 0.345 0.262 1.130 2.080 

1965 1.820 0.667 1.000 1.160 0.545 

1966 2.936 0.642 1.872 0.850 0.880 

1967 1.694 2.115 2.477 2.550 0.610 

1968 1.952 3.620 3.551 2.985 0.970 

1969 1.422 1.720 1.753 2.195 1.278 

1970 1.805 1.815 3.198 3.431 3.740 

1971 0.562 1.263 2.787 1.430 1.430 

1972 0.336 1.335 3.001 1.170 1.840 

1973 0.708 2.125 0.739 0.961 1.080 

1974 0.239 2.090 0.322 3.010 1.000 

1975 4.350 1.710 1.292 2.570 0.530 

1976 16.585 4.790 0.247 4.382 0.790 

1977 1.730 3.465 1.912 2.110 

1978 1.404 1.050 1.988 1.156 1.880 

1979 2.878 1.283 1.780 1.942 1.780 

155 
Table 8. Significance tests (Chi2, error probabilities in %) of the immediate 

or the delayed impact due to defoliation of the larch by the LBM on 

the fluctuations of the guild members (for further explanation see 

text). 

Immediate res~onse Dela~ed res~onse 

Yes No %p Yes No %p 

Exapate duratella 13 2 0.45 14 1 0.08 

Oporinia autumnata 11 4 7.07 9 6 43.86 

Pt. aeriferana 10 5 19.67 10 5 19.67 

Spilonota laricana 5 10 19.67 10 5 19.67 

Teleia saltuum 8 7 79.63 8 7 79.63 

Pristiphora laricis 11 4 7.07 8 7 79.63 

By examining possible immediate and delayed effects of defoliation on the fluctuation patterns of 

the individual species, one obtains a more revealing insight (Table 8). For ease of interpretation, the 

fluctuation patterns of the six species are compared to the LBM cycle in the Oberengadin (Z. diniana: 

mean density 58.31 larvae/kg; coefficient of variation (CV) 167 percent), as shown in Figs. 2a and 2b. 

1) Exapate duratella. Mean density 0.88 larvae/kg. Exhibits a cycle synchronous to the LBM 

and of large amplitude (CV 194 percent). The hypothesis of a significant immediate 

impact is accepted (p < 0.01 ), but there is also a highly significant delayed impact 

(p < 0.10). In two of the three cycles, E. duratella exhibits the highest densities of all 

associated species. 

2) Oporinia autumnata. Mean density 0.65 larvae/kg; CV 85 percent. In all three LBM 

cycles, the immediate impact is apparent, but there are three more minor peaks 

asynchronous with the LBM maxima. This suggests that processes other than the 

interspecific impact of the LBM (immediate impact: p = 0.07), but of similar efficiency, 

regulate the densities of 0. autumnata. In the Brian~onnais, maximal densities of 

0. autumnata are observed when LBM densities range from 0.3 to 36 larvae/kg. 

3) Ptycholomoides aeriferana. Mean density 0.009 larvae/kg; CV 136 percent. The fluctuation 

of the Engadine population suggests coincidence with the LBM cycle, but because in 15 

out of 28 years no larvae were recorded, no further comment is made. 

4) Spilonota laricana. Mean density 0.07 larvae/kg; CV 70 percent. The species fluctuates at 

a minor amplitude, so the hypothesis of an immediate impact has to be rejected 

(p = 0.20), whereas the hypothesis of a delayed impact shows an error probability of only 

0.07, inclining one toward acceptance. 

5) Teleia sa/tuum. Mean density 0.07 larvae/kg; CV 105 percent. Population increases and 

decreases alternate rapidly and independently of the LBM densities, so both impact 

hypotheses have to be rejected (p = 0.80). 

156 
Exapate duratella I LBM 

, 

i ,...: 

1960 1970 1980 

Oporinia autumnata I LBM 

Ptycholomoides aeriferana I LBM 

1000~----------~----------~--------~ 

.001~~--~----~----~----~--~~--~ 

1950 1960 1970 1980 

Figures 2a. Fluctuation patterns of guild members on larch from five 

subalpine regions in the European Alps (•••••) compared with the fluctuations 

of the larch bud moth (LBM) (o----o) and the relevant species (•----•) in the 

Oberengadin from 1952 to 1979. Sampling unit: larvae/kg larch twigs. 

157 
()) 

.X: 

........ 

Q) 

ro 

> 

... 

~ 

Spilonota laricana I LBM 

.001~----~----r---~~---+----~--~ 

1950 1960 1970 1980 

Teleia saltuum I LBM 

.001,_----~----~----~---4----~----~ 

1950 1960 1970 1980 

Pristiphora laricis I LBM 

100 

.001~----~----r-----r---~----~----~ 

1950 1960 1970 1980 

Figures 2b. Fluctuation patterns of guild members on larch from five 

subalpine regions in the European Alps (•••••) compared with the fluctuations 

of the larch bud moth (LBM) (o----o) and the relevant species (•----•) in the 

Oberengadin from 1952 to 1979. Sampling unit: larvae/kg larch twigs. 

158 
6) Pristiphora laricis. Mean density 1.54 larvae/kg; CV 73 percent. The fluctuation of PI in 

the Engadine (Fig. 2b) suggests that an immediate impact is exerted by the LBM, i.e. the 

density of PI is reduced already during the year of defoliation from that of the previous 

generation. This tendency is confirmed when all the data from the alpine arch 

(p = 0.07) are considered, whereas the hypothesis of a delayed impact is a chance event 

(p = 0.80). 

CONCLUSIONS 

Analysis of an immediate and a delayed interspecific impact of defoliation of the larch by the 

LBM on the fluctuation of six guild members reveals that out of 12 possible cases only the two related 

to E. duratella are significant (p < 0.01 ), and two more cases show a mere "close to significant" 

probability. In spite of methodological constraints, such as the evaluation of densities related to the 

biology of the LBM and not related to the individual species, or the grossly generalized assumption of 

the near to complete defoliation of larch forests over large areas, this result is surprising. Although 

comparison of the fluctuation curves clearly shows a parallel negative population trend (with the 

possible exception of T. sa/tuum), the nonsignificance is due to the asynchrony in population trends 

with the cycle of the LBM. This asynchrony is caused by the fluctuations at much lower densities 

which result in smaller amplitudes. Maximal densities of Oporinia, Ptycholomoides, Spilonota, and 

Pristiphora, which correlate with minimal densities of the LBM or densities well below defoliation 

threshold, suggest that these guild members are not regulated by interaction with the food quality. 

This conclusion was confirmed on two occasions when the LBM failed to transgress the defoliation 

threshold--in the Valle Aurina in 1973 and 1975 (Fig. 3) and Goms in 1972--but the guild members 

did not deviate from their general pattern of fluctuation. Furthermore, it is interesting to note that, 

with the exception of Exapate, trends indicating an interspecific impact (Oporinia and Pristiphora) are 

related to the immediate impact, i.e. to the lack of food and loss of shelter, but not to the delayed 

impact due to reduced food quality. 

Clearly, the folivore guild feeding on larch trees may be classified into two groups: those 

species which respond to the self-induced change in food quality by a drastic decline in population 

(LBM and Exapate); and those species which lack such a specific response (Oporinia, Ptycholomoides, 

Spilonota, Teleia, and Pristiphora). This finding is next discussed as a function of the plant 

carbon/nutrient balance (Bryant et al. 1988, Tuomi et al. 1988). 

Aspects Relevant to the Host Plant 

A pioneer species, Larix decidua has evolved in harsh climates and environments of low 

productivity which make for inherently slow growth and are thought to favor the evolution of 

constitutive antiherbivore defenses (Bryant et al. 1988). Unfortunately, allelochemicals have not yet 

been investigated in larch needles, but several other criteria serving as food value indices, such as 

growth rate (Baltensweiler 1984, 1985) and nitrogen and fiber concentrations (Benz 1974, Omlin and 

Herren 1976), are known to be strongly correlated with growth responses of the larch to abiotic or 

biotic constraints. As water consumption, photosynthetic capacity, and nitrogen concentrations are 

positively correlated with each other, the growth rate of needles responds immediately to the prevailing 

weather conditions. Consequently, growth conditions and nitrogen concentrations are reflected in an 

integrated manner by the shape of the growth curve and the final length of the needles (Fig. 4). Much 

more drastic effects on the physiology of the tree are to be expected from defoliation. Late frosts in 

spring may kill the new needle biomass and necessitate refoliation, whereas early frosts in fall may 

destroy needles and prevent the resorption of nutrients into the stem. In either case the flush of 

needles in the following spring remains short and stiff. Precisely the same effects are observed after 

artificial and/or natural defoliation by the LBM (Benz 1974, Omlin 1980, Baltensweiler 1985). The 

reduced food value of such needles for lepidopteran larvae is due not only to the physical properties of 

the needles, but also to their reduced nitrogen content (Benz 1974, Fischlin and Baltensweiler 1979, 

159 
Omlin 1980). These effects are all in agreement with the predictions derived from the model of plant 

carbon/nutrient balance (Tuomi et al. 1988). 

Aspects Relevant to the Insects 

LBM and E. duratella display the highest mean densities in the subalpine forests. They both 

show developmental and behavioral adaptations to low temperatures--LBM in the egg stage (Bakke 

1969) and E. duratella in oviposition (Baltensweiler 1961)--which enables them to cope successfully with 

the harsh subalpine environment. But even more relevant in this context are characteristics such as 

the early hatching, and the feeding of the first two instars close to meristematic plant tissue, which 

reflects their adaptations to exploit one of the most nitrogen-rich food resources in the subalpine 

environment (Baltensweiler in prep.). 

In contrast to LBM and E. duratella, the four guild members Ptycholomoides, Spilonota, Teleia, 

and Pristiphora show highest mean densities on larch near Zurich at 600 m a.s.l. (Auer, unpubl.). 

Spilonota, Teleia, and Pristiphora are "late season species" (Fig. 1), which means in general that they are 

obliged to be much more tolerant of low food quality, considering the usual maturational decline in 

foliar nutrients (Clancy et al. 1988). It is thus not at all surprising that reduced nutritional quality of 

larch foliage due to LBM defoliation does not constrain the population dynamics of these guild 

members appreciably. In accord with this conclusion is the finding that the trends in interspecific 

impact due to LBM defoliation (Oporinia and Pristiphora) are due more to the immediate impact, 

which is mainly quantitative lack of food and loss of shelter, and not to the delayed impact, which 

consists of reduced food quality. These findings, then, allow us to conclude that the trophic 

interrelation between larch and the two food specialists LBM and E. duratella may be interpreted as an 

adaptation of the insects to the physiologic responses of the larch to its abiotic environment. Thus the 

hypothesis of a quantitative defense reaction of the larch tree to the impact of specialistic herbivores 

would violate rules of parsimony. 

No specific and detailed studies have been made to determine the processes which might 

regulate the various guild members on larch in the subalpine region. Information on the fecundity of 

subalpine populations is scarce (e.g. P. aeriferana 51.8 ± 5.08 eggs/female, n = 6). Polyphagy and 

voltinism would be important mechanisms to buffer the various species against negative impact by the 

LBM. Parasitism of the guild members has been investigated in order to evaluate their possible role 

as alternative hosts to Z. diniana (DeLucchi et al. 1974, Lovis 1975). Eighty-one species of parasitoids 

have been obtained from eggs, larvae, and pupae of the associated species. Twenty-nine of these 

species also parasitize the LBM, but at a very insignificant rate. One hundred and nine species of 

primary and secondary parasitoids are known from LBM in the European Alps. However, since its 10 

most important parasitoids are monophagous, they cannot exert any direct regulative influence on the 

population dynamics of the guild members (DeLucchi 1982). 

We may conclude that five of the six most important species belonging to the folivore guild on 

Larix decidua exhibit population dynamics remarkably independent from the apparently dominant 

fluctuation cycle of the LBM. These five species have evolved as trophic generalists, whereas the LBM 

and E. duratella have apparently specialized to exploit the most nutritive niche available. Given the 

longevity of the larch, defoliation by the LBM does not have an excessively detrimental effect on the 

population dynamics of its host plant. On the contrary, it could be argued that the larch and the 

biocoenose would on the whole profit from the faster recycling of the needle biomass and its nutrients. 

This argument needs to be considered by those who would contend that the physiologic reaction of the 

larch to defoliation is a defensive reaction to folivores which may have evolved through coevolutionary 

steps. 

160 
Exapate duratella I LBM- Valle Aurina 

1000------------r---------~----------~ 

.0014-----~----~--~----~----~----~ 

1950 1960 1970 1980 

Figure 3. Comparisons of the fluctuation patterns of Exapate duratella and 

the larch bud moth (LBM) in the Valle Aurina (legend as in Figs. 2a and 2b). 

mm 

30 

20 I Mittelstation 1800 m 

10 

1.5. 15.5. 1.6. 15.6. 1.7. 15.7. 

1.5. 15.5. t6. 15.6. t7. 15.7. 

Figure 4. Growth curves of larch needles (mm: x ± sx) in the Lungau at three 

altitudes in 1975 compared with the daily mean temperature (station Tamsweg, 

1021 m a.s.l., °C, min+ max/2). 

161 
SUMMARY 

Population data obtained from a larval census of the larch bud moth, Zeiraphera diniana, and six 

associated insects feeding on larch needles are presented for five subalpine regions in the European 

Alps. The fluctuations of these folivore guild members are analyzed vis-a-vis their response to the 

spectacular periodic defoliation of the larch forests by the larch bud moth. The tortricid species 

E. duratella suffers from a significant impact and exhibits, therefore, a cyclic fluctuation similar to that 

of the larch bud moth, whereas the other five guild members show a remarkable independence in their 

fluctuations. It is concluded that their population dynamics in the subalpine zone are not regulated by 

the variability of the trophic resource, but by different processes. The relationship between the folivore 

guild and the larch is considered in an evolutionary context. 

ACKNOWLEDGMENTS 

I would like to thank for their technical assistance Mrs. E. Frei and Dr. D. Rubli of the 

Institute of Plant Sciences, Division of Phytomedicine. This paper is contribution No. 124 of the 

Working Group for the Study of the Population Dynamics of the Larch Bud Moth of the Swiss 

Federal Institute of Technology, Zurich, Switzerland. 

LITERATURE CITED 

AUER, C. 1961. Ergebnisse zwOlfjAhriger quantitativer Untersuchungen der Populationsbewegung des 

Grauen Urchenwicklers Zeiraphera griseana Hubner (= diniana Guenee) im Oberengadin (1949-

1960). Eidg. Anst. Forstl. Versuchswes. Mitt. 37: 173-263. 

AUER, C. 1977. Dynamik von Urchenwicklerpopulationen Ia.ngs des Alpenbogens. Eidg. Anst. Forstl. 

Versuchswes. Mitt. 53: 71-105. 

BAKKE, A 1969. Extremely low supercooling point in eggs of Zeiraphera diniana (Guenee). Nor. 

Entomol. Tidsskr. 3: 81-83. 

BALTENSWEILER, W. 1961. Beitrag zur Oekologie von Exapate duratella HEYD. (Lepidoptera: 

Tortricidae). Mitt. Schweiz. Entomol. Ges. 34: 307. 

BALTENSWEILER, W. 1984. The role of environment and reproduction in the population dynamics 

of the larch bud moth, Zeiraphera diniana Gn. (Lepidoptera: Tortricidae ), p. 291-302. In Engels, 

W., Clark, W.H., Jr., Fischer, A, Olive, P.J.W., and Went, D.F., eds. Advances in Invertebrate 

Reproduction. vol. 3. Elsevier, Amsterdam. 

BALTENSWEILER, W. 1985. On the extent and the mechanisms of the outbreaks of the larch bud 

moth, Zeiraphera diniana Gn. (Lepidoptera: Tortricidae ), and its impact on the subalpine 

larch-cembran pine forest ecosystem. In Turner, H. and Tranquillini, W., eds. Establishment and 

Tending of Subalpine Forest: Research Management. Proc. 3rd IUFRO Workshop. 1984. 

P1.07-00. Eidg. Anst. Forst. Versuchswes. Ber. 270: 215-219. 

BALTENSWEILER, W. and FISCHLIN, A 1988. The larch bud moth in the Alps, p. 331-351. In 

Berryman, AA, ed. Dynamics of Forest Insect Populations. Plenum, New York. 

BALTENSWEILER, W., BENZ, G., BOVEY, P., and DELUCCHI, V. 1977. Dynamics of larch bud 

moth populations. Annu. Rev. Entomol. 22: 79-100. 

162 
BENZ, G. 1974. Negative Rtickkoppelung durch Raum- und Nahrungskonkurrenz sowie zyklische 

VerAnderung der Nahrungsgrundlage als Regelprinzip in der Populationsdynamik des Grauen 

Urchenwicklers, Zeiraphera diniana (Guenee) (Tortricidae: Lepidoptera). Z ang. Entomol. 

76: 31-49. 

BIDAUD, P. 1970. Contribution a l'etude des geometrides du meleze. Travail de diplOme. Institut 

d'Entomologie, ETHZ 76 p. (unpubl.) 

BOVEY, P. 1978. Spilonota und Zeiraphera, p. 153-177. In Schwenke, W., ed. Die ForstschAdlinge 

Europas. 3. Schmetterlinge. Verlag Paul Parey, Hamburg. 

BRYANT, J.P., TUOMI, J. and NIEMELA, P. 1988. Environmental constraint of constitutive and longterm inducible defenses in woody plants, pp. 367-389. In Spencer, K.C., ed. Chemical Mediation 

of Coevolution. Academic Press, New York. 609 p. 

CLANCY, K.M., WAGNER, M.R., and TINUS, R.W. 1988. Variations in nutrient levels as a defense: 

identifying key nutritional traits of host plants of the western spruce budworm, p. 203-214. In 

Mattson, W.J., Levieux, J., and Bernard-Dagan, C., eds. Mechanisms of Woody Plant Defenses 

Against Insects: Search for Pattern. Springer-Verlag, New York. 

DELUCCHI, V. 1982. Parasitoids and hyperparasitoids of Zeiraphera diniana On. (Lepidoptera: 

Tortricidae) and their role in population control in outbreak areas. Entomophaga 27: 77-92. 

DELUCCHI, V., RENFER, A, and AESCHLIMANN, J.-P. 1974. Contribution a Ia connaissance des 

lepidopteres associes au meleze en haute altitude et de leurs parasitoides. La Rech. Agron. 

Suisse 13: 435-451. 

ELLENBERG, H. and KLOTZLI, F. 1972. Waldgesellschaften und Waldstandorte der Schweiz. Eidg. 

Anst. Forstl. Versuchswes. Mitt. 48: 589-930. 

FISCHLIN, A and BALTENSWEILER, W. 1979. Systems analysis of the larch bud moth system. 

Part 1: the larch-larch bud moth relationship. Mitt. Schweiz. Entomol. Ges. 52: 273-289. 

KALIN, A and AUER, C. 1954. Statistische Methoden zur Untersuchung von Insektenpopulationen. 

Z ang. Entomol. 36: 241-282, 423-461. 

LOVIS, C. 1975. Contribution a l'etude des tenthredes du meleze (Hymenoptera: Symphyta) en 

relation avec revolution dynamique des populations de Zeiraphera diniana Guenee (Lepidoptera: 

Tortricidae) en Haute-Engadine. Mitt. schweiz. Entomol. Ges. 48: 181-192. 

MATTSON, W.J., LAWRENCE, R.K., HAACK, R.A, HERMS, D.A, and CHARLES, P.-J. 1988. 

Defensive strategies of woody plants against different insect-feeding guilds in relation to plant 

ecological strategies and intimacy of association with insects, p. 3-38. In Mattson, W.J., Levieux, 

J., and Bernard-Dagan, C., eds. Mechanisms of Woody Plant Defenses Against Insects: Search for 

Pattern. Springer-Verlag, New York. 

OMLIN, F.X. 1980. Aspekte zum wechselweisen Beziehungsgefiige Uirchenwickler (Zeiraphera diniana 

On.) und Uirche (Larix decidua Mill.). 1. Teil: Einflussnahme des Uirchenwicklers auf die 

Uirche. Mitt. schweiz. Entomol. Ges. 53: 379-399. 

OMLIN, F.X. and HERREN, H.R. 1976. Zur Populationsdynamik des Grauen Uirchenwicklers, 

Zeiraphera diniana Guenee (Lep., Tortricidae), im Ahrntal (Stidtirol, Italien): Lebenstafeluntersuchungen und NahrungsverhAltnisse wahrend der Vegetationsperiode 1975. Mitt. Schwei~ 

Entomol. Ges. 49: 203-228. 

163 
RAIGORODSKAYA, I.A 1963. On the outbreak of mass multiplication of S. diniana in Eastern 

Sayan, 1960-62, p. 13-18. In Sb. Vrediteli lesov v Pridaijal'e Irkutsk. (In Russian.) 

ROOT, RB. 1967. The niche of exploitation pattern of the blue-grey gnatcatcher. Ecol. Monogr. 

37: 317-350. 

TENOW, 0. 1972. The outbreaks of Oporinia autumnata Bkh. and Operophthera spp. (Lepidoptera: 

Geometridae) in the Scandinavian mountain chain and northern Finland, 1862-1968. suppl. 2 

Zool. Bidr. Uppsala. 107 p. 

THOMANN, H. 1947. Exapate duratella Heyd. (Lepidoptera: Tortricidae). Ein spltfliegender Wickler 

der Graubiindner- und Walliser-Alpen. Mitt. schweiz. Entomol. Ges. 20: 475-483. 

TUOMI, J., NIEMELA, P., CHAPIN, F.S., III, BRYANT, J.P., and SIREN, S. 1988. Defensive 

responses of trees in relation to their carbon/nutrient balance, p. 57-72 In Mattson, WJ., 

Levieux, J., and Bernard-Dagan, C., eds. Mechanisms of Woody Plant Defenses Against Insects: 

Search for Pattern. Springer-Verlag, New York. 

164 
OUTBREAK OF ZEIRAPHERA RUFIMITRANA 

ON SILVER FIR 

HITHERTO UNKNOWN IN SOUTHWEST GERMANY 

HERMANN BOGENSCHUTZ 

Forest Research Station 

D-7800 Freiburg, Germany 

INTRODUCTION 

The most important defoliator of the silver fir, Abies alba, is Choristoneura murinana 

(Lepidoptera: Tortricidae) (Bogenschutz 1978). The fact that Zeiraphera rujimitrana H.-S. (Lepidoptera: 

Olethreutidae) (Bovey 1978) often occurs simultaneously with C. murinana has, in practice, frequently 

led to misidentification. The larvae of both species feed exclusively on juvenile needles in the upper, 

sun-exposed tree crowns and cause an identical type of defoliation. Foraged needles discolor reddishbrown in the early summer and are later shed. Once the brown needles have been shed, one can 

assess the severity of the infestation, over the course of previous years as well as more recently. 

Damage inflicted by the two species can be distinguished on the basis of morphological and behavioral 

differences between them. In this paper I present the results obtained from studies pursued since an 

outbreak of Z. rujimitrana in the Black Forest in 1986. It represents the first outbreak of this 

particular pest observed in southwest Germany to date. 

METHODS 

The population dynamics of Z. rujimitrana can be determined in two ways: 1) indirectly, by 

appraisal of needle loss on yearly shoot orders, and 2) directly, by studies of population densities of 

various developmental stages. Both procedures have advantages and disadvantages. The indirect 

method is universally applicable, allowing a relatively large area to be surveyed quickly. The direct 

method can be applied only during a very short, specified time period and is highly work intensive. It 

is used to determine not only changes in population density but also the factors influencing population 

dynamics. 

Using the indirect method, we examined a stand on the western slopes of the Black Forest 

which had been severely damaged in 1988. The age of the trees in the stand ranges from 95 to 115 

years. The stand is comprised of 85 percent silver fir, the remainder divided between beech and oak 

and has an average height of 23 m. Sloping to the southeast, it lies at roughly 550 m above sea level. 

In the winter of 1988-89, two field assistants using binoculars appraised the degree of defoliation 

in the discernible portions of the crown. Damage estimates based on yearly growth were rated in three 

categories: 1) low, up to a maximum of 1/3 defoliation, 2) medium, up to a maximum of 2/3 

defoliation, and 3) high, up to complete defoliation. In addition to the stand thus assessed, a heavily 

infested selection forest with a high proportion of silver fir was singled out in the upper Black Forest 

BARANCHIKOV, Y.N., MATrSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

165 
region, at about 850 m above sea level. In both of the stands, direct methods were used to collect 

data on population dynamics. To determine the density of the hibernating eggs, it is necessary to fell 

the sample tree. Sample branches from the upper crown area were then searched for eggs under the 

microscope. To determine the density of the descending larvae, a procedure was used whereby funnel 

traps (0.25 m 2 ), whose containers were filled with litter and humus, were placed directly under the tree 

crowns. In 1989, the year our data were collected, the feeding period was completed in the first half 

of June. Larvae were collected from the crown on different dates during the feeding period to 

determine the degree of parasitism, either by dissection or by rearing. 

RESULTS 

In the forest district of Staufen the outbreak of Z. TUjimitrana began in 1986. The years 

following showed a steady increase in the number of trees attacked, the area of infested stands 

approximately 600 ha in 1988, and the intensity of defoliation (Fig. 1). The eggs were found singly or 

in small groups between the bud scales of the year's shoots and to a lesser degree, between the scales 

at the base of the male flowers. Shoots located in the upper half of the crown were favored. In the 

initial phase of the study, we removed branches from the uppermost eight to 12 branch whorls of four 

dominant or codominant trees and sampled 10 shoots, both middle and secondary, from each whorl. 

The number of eggs found on each branch whorl sampled fluctuated greatly (Fig. 2), especially 

in the two uppermost whorls. Below the eighth branch whorl a clear reduction in egg numbers was 

found. As a result, the survey of fir stands will be limited to the third through seventh whorls, thereby 

yielding a sample of 5 x 10 = 50 shoots per tree. Table 1 shows that the rather consistent results 

obtained from four sample trees in the forest district of Staufen. In contrast, the results obtained from 

the forest district of St. Blasien showed greater variability. It must be noted that in the latter area, 

the old sampling method, examining the full upper crown, was still used. However, the order of 

magnitude of the results coincided in both regions. 

Less than half of the eggs found during the winter were intact and consequently developed to 

young larvae in the spring. On the average 8 or 11 percent respectively had a black discoloration. 

These eggs had been parasitized. The remaining eggs were empty (Table 2). 

Table 1. Egg density. 

Number Eggs/shoot 

Forest of sample 

district trees Min. Max. X s 

Staufen 4 10.2 13.7 12.3 1.6 

St. Blasien 9 4.0 13.3 7.4 3.6 

166 
-;/- 100 

.s: 

0' 

c 

:.0 

OJ 

OJ 

-

>-

.0 50 

"0 

ClJ 

..... 

, 

0 

-OJ 

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l/1 

ClJ 

QJ 

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~ 

.£ 

0' 

c 

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1986 

o! 100 

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Defoliation degree 

1988 

Defoliation degree 

1987 

Defoliation degree 

D low 

~ medium 

high 

Figure 1. Increasing defoliation by Zeiraphera rufimitrana in the forest 

district of Staufen. 

Table 2. Condition of the eggs. 

Ratio (%) 

Forest Number 

district of eggs Healthy Paras. Empty 

Staufen 4085 29.8 8.4 61.4 

St. Blasien 3514 42.7 10.9 46.4 

167 
150 

(/) 

01 

01 

(1) 

-0 100 '-a, 

.0 

E 

::l 

z 

----------------=--------- __________________________ 

-_-,:-_-__________ .,:-_-___ _ _________________________ 

-,:_-___________________ _ -----_-..:-_-_____________ _ ------------~---------: -:...------=------------------- __________________________ 

___________________________ 

_________________________ 

:-_- ------------_-_--:..,-_- _____________________ _____ _ _ 

:----------------------~-

·------------------------

~======================~ ________________________ 

-------:..--------------~­ =----.:---------------------

----:...--------~--------- --------------=-----:---...: 

5 10 

Branch whorl assessed from the top 

Figure 2. Distribution of the egg density (eggs/shoot) of Zeiraphera 

rufimitrana within the crown of four individual silver fir trees (whorl 1 was 

uppermost). 

Table 3. Density of the descending larvae. 

Forest 

district 

Staufen 

St. Blasien 

Number of 

funnel traps 

45 

9 

Larvae;m2 

15 

110 

168 
Althm~h egg density did not differ much in the two study areas, the number of descending 

larvae per m sampled at Staufen was only 14 percent of the amount sampled at St. Blasien (Table 3). 

Although parasitoids have been found to be important factors in the mortality of the larvae, 

they are not responsible for the different population declines. At least two hymenopterous species 

produced notable degrees of parasitization, reaching almost 60 percent (Table 4), but they have yet not 

been identified. Species 1 is a parasitoid originating from former larval instars. It leaves the host 

during or prior to the fourth instar to spin a cocoon in the crown. Species 2 to 4 were found 

relatively seldom. Species 5--an ectoparasite of late larvae--had a degree of parasitization of up to 

50 percent. Parasitoids of pupae were also found. 

Table 4. Parasitization of the larvae (estimated by dissection). 

Total Frequency per species 

Forest Sampling Larval paras. in \ of the total 

district date ins tar (\) (\) parasitization 

Ll L2 L3 L4 L5 1 2 3 4 5 

Staufen 08/05/89 77 9 12 2 0 32 100 0 0 0 0 

24/05/89 0 0 13 74 13 43 92 0 0 8 0 

08/06/89 0 0 1 8 91 59 16 0 0 0 84 

St. Blasien 19/05/89 3 19 29 47 2 39 95 2 3 0 0 

29/05/89 0 0 17 61 22 40 93 0 7 0 0 

20/06/89 0 0 0 3 97 43 5 0 3 0 92 

DISCUSSION 

As with C. murinana, the regional distribution of Z. rujimitrana corresponds with the distribution 

of its host Abies alba. Since 1945 five outbreaks have been documented, occurring both within and 

outside the natural habitat of the silver fir (Fig. 3). These outbreaks have a noticeably broad 

elevational range, from sea level to 1400 m, and occupy an area extending from northern Germany to 

northern Italy, a fact which indicates that outbreaks of Z. rufimitrana are not site specific. That is 

further verified by the current outbreak in southwest Germany, where numerous isolated populations 

have been discovered, occurring in different growth zones each in tum possessing a broad range of site 

conditions (Fig. 4). The type of stand management applied, furthermore, had no influence on the 

outbreaks, which were detected both in even-aged monocultures and in mixed forests. Outbreaks can 

usually be found on mature and overmature trees. Defoliation occurs exclusively on the sun-exposed 

portions of the tree crowns. Because of its obvious attraction to warmth, we can assume that climatic 

conditions are a factor in outbreaks of Z. rujimitrana. Tests are currently being conducted to 

determine whether a positive correlation exists between extraordinary weather conditions and outbreaks 

of Z. rujimitrana. 

169 
Figure 3. Natural habitat of Abies alba (dotted area) and zones of outbreaks 

of Zeiraphera rufimitrana since 1945 (shaded black). 

The outbreak of Z. rufimitrana in the forest district of Staufen began in 1986, and a noticeable 

decline in the damage was observed in 1989. That means that the culmination of the defoliation in 

1987 and 1988 was followed by a collapse of the population in the fourth year of the outbreak. A 

clear population decline has been shown in the differences between the densities of the eggs and the 

larvae. Effective parasitism is one reason for this decline. Other factors may be the lack of synchrony 

of the larval hatching and the budding of silver fir, or the influence of predators, especially on the 

stages descending to or living on or in the ground. Future studies should concentrate on these factors 

about which we know little as yet. 

Another question to be studied arises from the empty eggs found in winter. Had the larvae 

already hatched in summer or fall, or had they been emptied by a predator? The fate of eggs prior to 

the winter is currently being researched. 

SUMMARY 

The first observed outbreak of Zeiraphera rufimitrana was recorded within the natural habitat of 

the silver fir in southwest Germany in 1986. The larvae feed exclusively on needles of May shoots. By 

assessing needle loss from preceding shoot orders, it is possible to reconstruct the course of the 

outbreak. The peak of the outbreak was observed in two districts within the Black Forest in 1988. 

Although egg counts reached 12.3 and 7.4 eggs per shoot respectively in the two districts, only 15 and 

170 
• .. .. JIJ .. - Ftl • At.\, WalduhuU 

Figure 4. Growth zones of Baden-Wurttemberg and a real distribution of 

Zeiraphera rufimitrana outbreaks (hatched area) since 1987. 

110 larvae per m2, respectively, reached the pupal stage. Parasitoids accounted for a substantial 

portion of the decrease in population density, with a mortality rate of 8 to 11 percent of the eggs and 

43 to 59 percent of the larvae parasitized. Additional factors relating to mortality are discussed. 

LITERATURE CITED 

BOGENSCHUTZ, H. 1978. Tortricidae. In Schwenke, W. Die Forstsch!dlinge Europas, p. 55-89. 

3. Band: Schmetterlinge. Verlag Paul Parey, Hamburg, Berlin. 

BOVEY, P. 1978. Spilonota und Zeiraphera. In Schwenke, W. Die Forstsch!dlinge Europas, p. 153-177. 

3. Band: Schmetterlinge. Verlag Paul Parey, Hamburg, Berlin. 

171 
AN INSECf OUT OF CONTROL? 

THE POTENTIAL FOR SPREAD 

AND ESTABLISHMENT OF THE GYPSY MOTH 

IN NEW FOREST AREAS IN THE UNITED STATES 

MAX W. McFADDEN and MICHAEL E. McMANUS 

USDA Forest Service 

Northeastern Forest Experiment Station 

100 Matsonford Road 

Radnor, PA 19087 U.S.A 

USDA Forest Service 

Northeastern Forest Experiment Station 

51 Mill Pond Road 

Hamden, Cf 06514 U.S.A 

INTRODUCTION 

The gypsy moth, Lymantria dispar L., was introduced from Europe into North America near 

Boston, Massachusetts, in 1869, and is now well established as a serious defoliator of forest, shade, and 

fruit trees over much of the eastern United States. Despite substantial efforts to eradicate, contain, or 

control this pest, the gypsy moth has persisted and continues to extend its range. The generally 

infested area currently extends from the northeast comer of North Carolina along a diagonal line that 

extends through Virginia, West Virginia, and the northeast comer of Ohio into Michigan. These five 

states are referred to as the transition zone, and states to the east of this line represent what is 

referred to as the generally infested area. A vast area of suitable habitat for the gypsy moth, much of 

which is valuable commercial hardwood forest, lies to the south and west of the generally infested area. 

This paper assumes that the gypsy moth will if not checked expand its range into that area and 

therefore proposes a management strategy for preventing this from occurring. 

THE HISTORICAL RECORD 

The original infestation increased and spread gradually until, by the summer of 1889 (30 years 

after its introduction), the insect was so abundant and destructive that it attracted public attention. 

The first outbreak encompassed forested lands that included 30 towns and cities in the greater Boston 

area and prompted the state of Massachusetts to implement an intensive program to eradicate the 

insect. The program was so successful in reducing the infestation that the state legislature chose to 

abandon the effort in 1900. Many people considered that action to be a fatal mistake. 

During the next 5 years, gypsy moth populations increased tremendously in Massachusetts and 

new infestations were subsequently discovered in the neighboring states of Rhode Island, New 

Hampshire, Vermont, and Connecticut. From 1906 to 1912, the federal government financed the 

importation of natural enemies of the gypsy moth from several European countries and from Japan 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

172 
(Brown and Sheals 1944). Efforts to prevent the shipment of gypsy moth-infested products into 

outlying areas were intensified and led eventually to enactment of a federal domestic quarantine against 

the insect in 1912. The quarantine has been modified over the years, but remains in effect today and 

credited with greatly reducing the accidental long-range transport of gypsy moth on regulated 

commodities. 

Between 1906 and 1920, the gypsy moth spread westward at an estimated rate of 9.6 km a year. 

Isolated infestations were discovered on estates in New York, New Jersey, and Ohio. In 1923, a 

barrier zone extending from Canada to Long Island and encompassing some 27,300 km2 was 

established through a cooperative effort by the federal government and the state of New York to 

prevent the westward spread of the insect. Infested territory to the east of the zone was to be treated 

by the responsible state; infestations found within and to the west of the barrier zone were to be 

eradicated. Despite these efforts, the barrier zone became generally infested by 1939, and the effort 

was terminated in 1941. 

Gypsy moth infestations seemed to explode in 1951-52, when 0.6 million ha were defoliated, as a 

result of which yet another thorough appraisal of the problem was made by state and federal officials. 

A seven-point plan to re-establish the barrier zone was formulated in 1953, and the Congress 

made funds available to initiate an eradication program using DDT in 1956. By 1958, defoliation by 

the gypsy moth was recorded on only 50 ha within the totally infested area. However, concerns about 

the environmental persistence of DDT became paramount and use of the chemical was discontinued. 

Hopes of eradicating the gypsy moth were abandoned and a long-overdue emphasis was placed on 

research. The areas of infestation and defoliation increased substantially thereafter, which provided 

impetus for accelerated programs of research on the gypsy moth beginning in 1971 and continuing to 

the present. 

MEANS OF SPREAD 

Current distribution and spread of the gypsy moth in the United States (Fig. 1) is a product of 

both the natural spread of wind-blown first-stage larvae, and the inadvertent human transport of life 

stages from the generally infested area throughout the U.S. Historically, the extent of artificial 

introduction has probably been underestimated and the significance of natural spread overestimated. 

The following discussion offers a synthesis of what is known about both methods of spread. 

Windblown Dispersal of Larvae 

The distance that newly hatched larvae can disperse has been a controversial question for years. 

Early workers were convinced that long-distance dispersal of larvae was widespread in the Northeast 

and that larvae were readily blown up to 40 km by the winds (Collins 1917). However, Mason and 

McManus (1981) concluded that in nonmountainous terrain 99 percent of airborne larvae would be 

deposited within one km of their source. Even in mountainous areas, where mechanical turbulence 

and updrafts are more pronounced, an atmospheric dispersion model predicted that most larvae would 

be deposited within 3 km downwind. 

Taylor and Reling (1986) conducted extensive aerial sampling of first-stage larvae over heavily 

infested ridges in Pennsylvania and suggested that 0.3 percent may get the opportunity to travel up to 

19 km in one episode. More recently, Fosberg and Reling (1986) modeled the dispersal of gypsy moth 

larvae in mountainous terrain using a three-dimensional wind and dispersion model with real time 

climatological data from coastal California. Their model predicted that larvae would be carried aloft 

and transported more than a few hundred meters in only 2 percent of the cases. When long-range 

transport did occur, larvae were deposited 7 to 21 km away, but in very low concentrations. The 

173 
~Transition Zone 

Generally Infested Area 

Figure 1. Current gypsy moth distribution 

evidence suggests that although some larvae may be transported long distances when source populations 

are dense and hatch periodicity and optimal meteorological conditions are synchronized, most larval 

dispersal is a relatively short-range phenomenon. Support for this conclusion can be found in the 

documented record of isolated infestations that have occurred beyond the generally infested area. Of 

more than 264 isolated infestations that have been detected by the Animal and Plant Health Inspection 

Service, only 47 (18 percent) exceeded ca. 2.6 square km (1 sq mi) in area, even though these incipient 

populations may have persisted for several years prior to their detection. This suggests that under 

normal circumstances, the extent of larval dispersal and subsequent survival is minimal. 

We recognize however that the Appalachian mountain range has been a factor in the accelerated 

rate of natural dispersal of the gypsy moth to the south. Susceptible ridgetop stands favor gypsy moth 

reproduction and survival, and complex wind fields associated with mountainous terrain increase the 

probability of greater dispersal. In the generally infested area, larval dispersal probably accelerates the 

redistribution and coalescence of local populations that have already begun to increase over broad 

areas. 

Inadvertent Introduction of Life Stages 

State and federal officials recognized in the early 1900s that spread of the gypsy moth out of the 

infested area around Boston was expedited by the transport of egg masses and other life stages on 

vehicles and commodities carried by major roads and thoroughfares. This led to enactment of a federal 

quarantine against the insect in 1912. Despite that regulatory effort, infestations were again discovered 

far beyond the infested area. In retrospect, it appears that the gypsy moth was probably introduced 

174 
and reintroduced into both contiguous and distant areas and yet went undetected since there were no 

pheromone traps in those years and scouting for egg masses at low densities was and is an imperfect 

science. 

The dimensions of the problem are best demonstrated by reviewing the circumstances of an 

isolated infestation detected in Somerville, New Jersey, in 1920. This infestation originated from a 

separate introduction of infested blue spruce trees from the Netherlands in 1910, prior to enactment of 

the federal quarantine. At the time it was discovered, the infestation was scattered over 1,040 km2 

around Somerville. A record of shipments of trees from the Somerville estate indicated that, prior to 

1921, 261 shipments had been sent to 15 states from Connecticut south to Florida and west to 

Minnesota and Missouri. Follow-up inspections revealed that the shipments had led to new 

infestations in at least three of the states. The Somerville infestation was finally eradicated in 1931 at 

a total estimated cost of $2.5 million (Felt 1942). When one considers that this incident involved only 

commodity originating from a single small infestation at a time when transportation was somewhat 

limited, one can better appreciate the magnitude of the task to contain the gypsy moth today. 

The regulatory quarantine is still in effect, although it has been modified over time to emphasize 

detection of life stages in commercial household moves. Historically, most new infestations have been 

traced to the transport of life stages on backyard furniture and related articles (dog houses, firewood, 

recreational equipment). Under new regulations implemented in 1983, shipments of household goods 

from designated high risk areas through or into nonregulated areas must be inspected at the point of 

origin and certified free of gypsy moth life stages. 

Since 1980, California officials have initiated an aggressive program to supplant the federal 

quarantine on gypsy moth since they see the insect as a serious threat to the fruit and nut industry in 

the state. The California Department of Food and Agriculture maintains 16 border stations where 

personnel conduct inspections of recreational vehicles (campers, motor homes, boat and house trailers) 

entering the state and identify shipments of household goods from states known to be infested by the 

gypsy moth. Recreational vehicles are known to be carriers of gypsy moth life stages. A survey 

conducted by APHIS in 1980 determined that 33 percent of all RVs leaving seven infested New Jersey 

campgrounds were carrying gypsy moth life stages. Under the California program, shipments of 

household goods are allowed to proceed through the border station but inspection of all outdoor items 

is conducted by destination county commissions after the moving van is unloaded. Documented results 

of this program are dramatic in that they illustrate the enormous potential for artificially introducing 

the gypsy moth into one of the most distant states from the generally infested area (Fig. 2). More 

than 2,000 interceptions of gypsy moth life stages from 14 states and Canada have been recorded since 

the program began in 1980. Most of the border interceptions occurred on recreational vehicles, 

although from 70 to 210 interceptions annually were recorded from county inspections of household 

goods at their destination. Egg masses were the life stage most frequently encountered, and in 

approximately 38 percent of the cases the life stages encountered were viable. As a result of this 

concerted effort to exclude the gypsy moth from California, the number of established infestations 

requiring treatment with pesticides declined from 10 in 1983 to only one in 1987, thus saving 

California taxpayers millions of dollars in treatment costs. The state estimated the cost of chemically 

treating the 10 infestations identified in 1983 at $1.5 million. 

The increasing number of interceptions recorded since 1980 is obviously related to the extent 

and severity of the initial infestation in the generally infested area (Fig. 3). The number of 

interceptions recorded annually on recreational vehicles at California border stations, coupled with the 

fact that from 26 to 30,000 shipments of household goods from infested areas have been logged 

annually since 1984, demonstrates the potential for introduction of the gypsy moth into previously 

uninfested states (Fig. 4). These data also suggest that the gypsy moth is repeatedly being introduced 

into states both adjacent to and far removed from the generally infested region. 

175 
Since 1978, pheromone traps have been used extensively to detect isolated infestations 

throughout the United States and serve as the basic tool of the regulatory program. When pheromone 

traps are deployed according to APHIS protocols (1 trap/9 sq mi, depending on the terrain, setting, 

whether forest or residential, and so forth), new infestations are frequently detected and delimited 

within 2 to 3 years of their establishment and can then be more readily eliminated. As mentioned 

earlier, 72 percent of new infestations are less than 2.6 km in area when they are delimited. Those 

more extensive infestations that have been discovered in recent years in the states of Oregon (1984), 

Idaho (1987), and Utah (1988) apparently went undetected for several years because those states did 

not deploy a systematic grid of pheromone traps. The success of state detection programs is 

-~--_<:Q_n_!i_!!g@_l__ypQn the intensity of the trapping effort that each state initiates and maintains. 

FACfORS THAT LIMIT ESTABLISHMENT IN NEW AREAS 

Based on the statistics previously cited from the California gypsy moth exclusion program, there 

is no doubt that-gypsy-moth life stages have been transported to many uninfested states every year and 

- that the number of such incidents has increased dramatically since the 1980-82 outbreak in the 

generally infested area. Yet judging from the relatively small number of infestations that have occurred 

and -required APHIS to apply eradication treatments, we have to conclude that the probability of the 

gypsy moth becoming established in new areas is quite low. If this were not the case, the gypsy moth 

would by now, undoubtedly, have become entrenched in the oak-hickory and oak-pine forests 

throughout North America and in residential areas from coast to coast. 

HOST AVAILABILITY AND SUITABILITY 

In this section we attempt to elucidate those factors tl;lat affect the establishment of gypsy moth 

in new areas and will ultimately determine the future distribution of the insect in North America. 

Unlike most other forest defoliators, the gypsy moth is a polyphagous insect that can feed 

successfully on over 200 species of trees that grow in the continental United States. Historically, 

however, outbreak areas have been characterized by an abundance of preferred host species, mainly 

oaks and aspen. Given the known distributions of oak-hickory and oak-pine types in the United 

States, the gypsy moth has the potential for establishing itself and thriving in several states to the 

south and west of the current generally infested area. The severity of the problem will be exacerbated 

by the availability of the contiguous forested area occupied by preferred food species, mainly oaks. 

The state of Pennsylvania, for example, contains over 4 million ha of oak forest, especially along the 

Appalachian mountain range that traverses the state. The state has experienced repeated outbreaks 

since 1970, as the gypsy moth has slowly spread to the south and west. Since oak remains the 

dominant species in Pennsylvania forests, the gypsy moth will be a recurring problem there in the years 

ahead. Similarly, the oak-pine forests on Cape Cod, Massachusetts, have sustained severe and repeated 

episodes of defoliation since the early 1900s and are still considered highly susceptible. Missouri, 

Tennessee, Kentucky, and West Virginia contain extensive areas of oak forests and have been identified 

as susceptible to the gypsy moth. The unglaciated regions of several midwestern states also contain 

extensive forests of oak and other susceptible species. 

States further west and south have not been considered at risk to the gypsy moth because in 

them coniferous forests predominate. Hardwood species, including oaks, are scattered throughout these 

forests, however, especially along the waterways, and there they offer a suitable habitat for the gypsy 

moth. A case in point is Lane County, Oregon, where in 1987, 121,000 ha of mainly Douglas-fir forest 

were treated to eradicate an extensive but isolated infestation of gypsy moth that went undetected for 

several years. This infestation was successfully eliminated over a period of 3 years during which 

state/federal agencies applied multiple Bt treatments to the residual population. 

176 
II Infested 

D Non Infested 

Introductions 

Figure 2. Introduction of gypsy moth into California 

We must emphasize that although host availability may restrict the geographical extent of the 

problem when the gypsy moth is introduced beyond the natural range of oak, most successful 

establishments in places far removed from the generally infested region occur in urban residential areas 

and result from the introduction of life stages on household goods. In these areas, extensive plantings 

of preferred food species such as oaks, aspen, and ornamental fruit trees can support the establishment 

and expansion of gypsy moth populations. 

Although considerable effort has been directed toward defining the range of host suitability for 

gypsy moth (Mosher 1915, Barbosa et al. 1983, 1986, Lechowicz and Mauffette 1986, Miller and 

Hanson 1989), most of these studies have been restricted to laboratory preference tests conducted on 

individual tree species common to the eastern United States. These studies confirm that although 

gypsy moth feeding preferences are extremely catholic, many tree species are not favored or rarely fed 

upon, such as black locust, Robinia pseudoacacia, ash, Frarinus spp., and yellow poplar, Liriodendron 

tulipifera. 

In general, the range of host suitability is narrowest for the early larval instars and broadest for 

the late larval instars, which can successfully feed and complete their development on most hardwoods 

and conifers. We do not fully understand the suitability of all species to all instars, especially when 

host switching occurs in the field. Gansner and Herrick (1985) reported on the preferences of gypsy 

moth for host species exhibited in the defoliation that occurred over a 5-year period on 575 plots in 

Central Pennsylvania. Although their data provide an index of preference, the results were somewhat 

compromised because less than half of the plots sustained moderate to heavy defoliation ( > 30 

percent), and that occurred in one year. Consequently, hemlock, a coniferous species readily defoliated 

177 
20 

tn 

CD 

'-u 

< 

..... 

0 10 

tn 

c 

0 

·-

== 

0 

1976 77 78 79 80 81 82 83 84 85 86 87 88 89 

Year 

Figure 3. Acres defoliated by gypsy moth 

by the gypsy moth and among which mortality often results, was the least preferred species in their 

study. This suggests that host preference in the field will be affected by initial distribution of the gypsy 

moth, relative density of the population, and proximity to other infested stands. There are still many 

unanswered and puzzling questions. For example, Barbosa et al. (1983) found that gypsy moth larvae 

reared on sweetgum, Liquidambar styracijlua, had the shortest developmental period, the highest pupal 

weights, and the largest mean fecundity, yet we observe mature native sweetgum trees in Maryland that 

are fully foliated while adjacent oaks are completely stripped. Obviously, more research is needed on 

gypsy moth/host plant relationships. 

OTHER FACTORS 

In addition to host availability and suitability, other variables such as climate, natural enemies, 

and losses due to dispersal affect the successful establishment of gypsy moth life stages that have been 

introduced into new areas. Given the known distribution of the gypsy moth worldwide (Giese and 

Schneider 1979), the insect is probably capable of surviving anywhere in the United States where 

178 
U) 

c 400 

0 

;; 

a. 

Q) 

(,) 

'-

Q) 300 .... 

c • RVS ,._ • HHGS 0 D TOTAL '- 200 

Q) 

.c 

E 

:J 

z 

100 

1980 81 82 83 84 85 86 87 

Year 

Figure 4. California interceptions from 1980-1987 

suitable hosts exist. The gypsy moth is distributed as far north as Leningrad (60 N), as far south as 

North Africa (30-32 N) and the Far East (20 N). However, the area where periodic outbreaks occur 

lies between 0 and 50 E. longitude and 40-55 N. latitude and typically receives 25-100 em of 

precipitation annually. Since the continental U.S. lies between 25 and 50 N. latitude, climate should 

not be a major factor limiting establishment by the gypsy moth. 

The gypsy moth has an obligatory egg diapause whereby the egg stage must experience a period 

of exposure to chilling below a threshold temperature (ca. 5°C) in order to satisfy diapause 

requirements prerequisite to successful eclosion. The egg stage is better protected against severe cold 

than against mild or fluctuating temperatures. Outbreaks have occurred as far north as southern 

Quebec, where Madrid and Stewart (1981) concluded that lack of hosts in the province to the north 

are more limiting to the insect than extreme winter temperatures. 

Experience with isolated infestations in the Pacific Northwest, Santa Barbara, California, and in 

Myrtle Beach, South Carolina, indicates that diapause requirements were satisfied in these climatically 

marginal areas. However, eclosion occurred much earlier in the spring and extended over a period of 

4 to 8 weeks. This fact complicates the timing of eradication treatments and usually warrants repeated 

applications of pesticides at intervals throughout the hatch period. 

179 
Although we know little about the fate of -gypsy moth life stages in new habitats, recently both 

parasitism and predation of life stages have been documented in instances where sterile insect releases 

were made to eradicate isolated infestations. In Berrien County, Michigan (1983), birds, especially blue 

jays, preyed heavily on releases of sterile male gypsy moths; in Bellingham, Washington (1985), where 

sterile eggs were released, 21 percent of the larvae collected had been parasitized by either Cotesia 

melanoscelus or Compsilura concinnata. Pending information from detailed studies, we can only assume 

that a complement of generalist parasites and predators or their ecological equivalents would attack the 

gypsy moth in isolated infestations. 

One would think that passive dispersal of first-stage larvae would result in a high incidence of 

larval mortality. Hatching larvae frequently rest on or near the egg mass for hours if not days without 

feeding when meteorological conditions are not conducive to their dispersal. The longer they are 

prevented by adverse weather from dispersing, the more subject they are to predation and the lower 

their chances of successfully establishing on suitable foliage. Periods of rain can also drown the firststage larvae. Windblown larvae must first survive the physical environment during the dispersal 

process, then locate and establish on suitable foliage after they are deposited. Airborne larvae are 

particularly vulnerable to desiccation. In a study by Taylor and Reling (1986), those larvae that had 

been collected aerially were all dead. Larvae deposited in hostile or nonforest environments obviously 

will not survive. The probability of establishment of those first-stage larvae that do reach forested 

environments is largely dependent upon the structure and composition of the vegetation in the area 

where they are deposited. Although estimates of gypsy moth mortality attributed to larval dispersal are 

not available, estimates are available for the eastern spruce budworm, another passively dispersed 

species. Miller (1958) estimated that the average mortality rate of first-stage budworm over a 6-year 

period was 64 percent and varied from 48 to 82 percent. Dispersal losses were greatest in open, 

mature stands and least in dense, middle-aged stands. 

Many if not most introductions of gypsy moth life stages do not produce new infestations, and 

many factors acting in concert probably contribute to the demise of the gypsy moth in these remote 

situations. This conclusion is supported by the relatively few isolated infestations that have been 

reported in the past 13 years despite the large number of artificial introductions that apparently occur 

annually in states as far removed as California. 

POTENTIAL IMPACT OF GYPSY MOTH ON FORESTS TO SOUTH AND WEST 

On review of the approximate range of the oak-hickory and oak-pine forests beyond the 

currently infested area, it is apparent that there is abundant, highly suitable gypsy moth habitat to the 

south and west. A workshop held in West Virginia in 1987--"Coping with the gypsy moth in the new 

frontier" --was organized to provide the latest information on forest effects and management strategies 

to forest managers in states along the advancing front. This update was deemed necessary because the 

forests in the "new frontier," the Appalachian region, contain both a large oak component and a more 

valuable timber resource than those previously inhabited by the gypsy moth. In order to understand 

the potential impact of the gypsy moth on forests, we must shift our thinking from effects on 

individual trees to effects on stands of trees. 

Stand Susceptibility 

The term "susceptibility" refers to the potential for a forest stand to be defoliated by the gypsy 

moth, while "vulnerability" is the probability of mortality occurring after a stand has been defoliated. 

Bess et al. (1947) classified forest stands in New England as susceptible or resistant to defoliation on 

the basis of species composition and their history of disturbance. Species composition is the single 

most important factor that determines a stand's susceptibility; the higher the basal area in oaks and 

other preferred species such as aspen and birch, the more susceptible is the stand. Houston and 

180 
Valentine (1977) recognized the need to identify in advance of the gypsy moth those forest stands that 

are likely to be defoliated often and those where tree mortality is likely to be significant. They used 

ordination techniques to compare forest stands based on certain structural tree features known to 

influence gypsy moth larval behavior and survival and larval host food preferences. Later, Valentine 

and Houston (1984) developed discriminant functions for identifying mixed-oak stand susceptibility 

based on the measurement of diameters of preferred host trees and those trees that possess deep bark 

fissures or bark flaps between the ground and 1.83 m (6 ft). Herrick and Gansner (1986) also 

developed a rating system based on the basal area of oaks and that of trees with good crown condition. 

Mason (1987) reviewed both rating systems and provided an in-depth discussion of the merits of both 

approaches. It is important to recognize that susceptible stands are probably defoliated both more 

frequently and more severely than stands designated as resistant. However, Bess et. al. (1947) noted 

that resistant stands can be defoliated if they are adjacent to susceptible ones; furthermore, resistant 

stands that incur severe defoliation can themselves become more susceptible. 

Stand Vulnerability 

Stands defoliated by the gypsy moth have incurred tree mortality, growth loss, and changes in 

understory composition (Hicks and Fosbroke 1987). The magnitude of these impacts depends upon the 

number and severity of defoliations on individual trees. When trees are defoliated 50 to 60 percent or 

more, they respond by refoliating in midsummer. This creates stress on trees and predisposes them to 

attack by secondary agents (other insects and pathogens) that are the direct cause of subsequent 

mortality. Other stresses such as drought or frost along with site and stand conditions and incidence 

of secondary organisms, contribute to tree mortality and complicate the task of predicting the 

vulnerability of individual stands. 

Although the results of studies to assess mortality after episodes of gypsy moth defoliation and 

to rate stand vulnerability have been somewhat variable, we can make some statements on which there 

is a consensus: 1) stands that contain the most oak incur the highest mortality; 2) trees that sustain 

two or more moderate to heavy defoliations (> 60 percent) are most likely to die; 3) trees with poor 

crown conditions are more vulnerable to defoliation than healthy trees; and 4) there is a "first wave 

effect" such that stands in newly infested areas realize the highest mortality rates after their first severe 

episode of defoliation. This pattern held true in New England (Campbell and Sloan 1977), New Jersey 

(Kegg 1973), and Pennsylvania (Quimby 1987) and appears likely to occur in the mid-Atlantic states of 

Maryland and West Virginia. 

It is difficult to compare the published results of these studies because losses are expressed 

variably as value loss per acre, volume of pulpwood and sawtimber, dead trees per acre, or basal area 

per acre. Campbell and Sloan (1977) summarized results from the first major outbreaks in New 

England (1911-1931) and reported that the mortality of oak was 48 percent of total basal area and 

ranged from minor losses to catastrophic losses in some stands. In the aftermath, species composition 

of the stands was altered; they contained fewer oaks and more nonfavored species. Gypsy moth 

outbreaks still occur in these stands, but do not result so much in mortality as in deterioration of 

growth, yield, and wood quality. 

The first severe outbreak in New Jersey occurred from 1968 to 1971 on the Newark watershed, 

where stands sustained 3 consecutive years of defoliation (> 75 percent). Net basal area loss was 

44 percent; by 1972 oak mortality had reached 63 percent and another 28 percent of stems was left in 

declining condition (50 percent or more of canopy dead). Gansner et al. (1983) and Herrick and 

Gansner (1988) measured changes in forest conditions after gypsy moth defoliation in northeastern and 

central Pennsylvania and concluded that oak basal areas were reduced in both areas, but that timber 

stands outgrew most losses. These studies concentrated on the effects of defoliation on timber volume 

and value over a broad resource area rather than on individual stands, and since less than 40 percent 

181 
of the plots in central Pennsylvania experienced even one year of moderate to heavy defoliation, 

mortality was properly not anticipated. 

In another Pennsylvania study, where appraisals were conducted only on forest land known to 

have sustained repeated defoliations and tree mortality, Quimby (1987) reported tree mortality rates of 

27.6 percent for pulpwood and 32.5 percent for sawtimber over nearly 350,000 acres, and 51.3 percent 

for both pulpwood and sawtimber over another 341,000 acres. Summer droughts during the period 

from 1980 to 1983 were thought to exacerbate the defoliation stress and resultant mortality. 

Preliminary reports on tree mortality in the ridge and valley system in western Pennsylvania and from 

the panhandle of West Virginia suggest that oak mortality is variable by species, but exceeds 25 percent 

in most areas (Twery, pers. comm. ). Collectively, these studies indicate that oaks are most vulnerable 

to gypsy moth defoliation and incur the highest mortality rates. However, there is no consensus on 

which species of oak are most affected nor on whether trees growing on poor, stressed sites are more 

vulnerable to defoliation than those occupying better, mesic sites. 

Although forest managers are primarily concerned about mortality, we should not discount the 

effects of defoliation on growth loss and regeneration. Hicks and Fosbroke (1987) have reviewed this 

subject and discussed the need to develop models from site and stand data that can predict mortality 

after episodes of defoliation. By linking stand vulnerability with susceptibility models, forest land 

managers can develop a basis for sound pest management decisions. 

As the gypsy moth moves into the oak-pine forests of the South and the mixed-hardwood stands 

of the Midwest, questions arise about the dynamics of the insect in these stands and its ultimate 

impact. Several midwestern states are using available susceptibility models to rate their stands in 

advance of the gypsy moth. Although the species composition of these stands is more diverse, the 

native oak species are similar to those found in the generally infested area; consequently, these models 

may adequately classify stand susceptibility. 

The picture in the South is more complex because oak-pine mixtures there consist of conifers 

and oaks that do not occur in the susceptible oak-pine stands of southern New Jersey and Cape Cod. 

At a recent conference on the management of pine-hardwood mixtures, presentations by Gottschalk and 

Twery (1989) and Montgomery et. al. (1989) synthesized what is known about the impact of gypsy 

moth on pine-oak stands to the north and discussed implications for management of these 

commercially important stands in the South. 

In 1988-89, the Gypsy Moth Research and Development Program funded several projects 

designed to evaluate the suitability of native southern species to the gypsy moth both in the lab and in 

field plots established along the advancing front of the infestation. Similar evaluations are being 

conducted in the highly susceptible native aspen stands of central Michigan. These studies will provide 

data needed by forest managers to assess the potential susceptibility and vulnerability of stands in newly 

infested areas. 

It seems likely that the gypsy moth will indeed continue to spread south and west until it runs 

out of suitable hosts. While large areas of southern pine will undoubtedly be resistant to defoliation, 

extensive commercial forest lands to the south and west of the currently infested zone are at 

considerable risk. Affected states must be prepared either to alter stand composition to reduce their 

susceptibility/vulnerability or to apply pesticide treatments more extensively than we are now capable of 

financing. If these management costs are deemed prohibitive, then we should consider initiatives to 

slow or even halt the spread of the gypsy moth in the immediate future. 

182 
CONTAINMENT: A VIABLE OPTION THEN AND NOW 

Historically, there has been considerable debate on the merits of instituting a containment 

policy. Detractors say that since the natural spread of the moth cannot be halted, containment efforts 

would be futile and, furthermore, the cost of such a program would be prohibitive. Proponents argue 

that every year that a state remains uninfested translates into savings in pest management costs and 

spares the citizenry a year's worth of nuisance and damage. 

Major programs have been undertaken to eradicate, control, or contain the gypsy moth since it 

was introduced into North America (Perry 1955). As mentioned earlier, the barrier zone that was 

deployed from 1923 to 1942 is credited with restricting distribution of the gypsy moth to New England 

east of the New York line. Felt (1942) estimated that maintenance of the barrier zone cost $210,000 

annually. In 1940, the chief of the Bureau of Entomology and Plant Quarantine commissioned a blue 

ribbon committee to conduct a thorough appraisal of the gypsy moth problem. The committee's report 

strongly urged maintaining the barrier zone to prevent the spread of the moth to the central hardwood, 

southern Appalachian, and Piedmont regions (Korstian and Ruggles 1941 ), but funding for the barrier 

zone was drastically reduced in 1941, when resources were redirected to the war effort. 

In 1952, a study group appointed by the Secretary of Agriculture initiated a program to 

assemble the facts needed for evaluation of the problem and for determining a future combative policy 

(Perry 1955). A seven-point plan for the prevention of spread and reduction in damage was 

formulated, including re-establishment of the barrier zone. The plan was implemented to the extent 

permitted by available funds, but eventually discontinued. In 1978 the Expanded Gypsy Moth Program 

initiated a contact with Ketron, Inc. to develop a cost/benefit analysis for gypsy moth containment. 

The report (Blacksten et al. 1978) concluded that significant expenditures are justified even to slow the 

spread of the moth and that the existing APHIS program projected a quite favorable benefit/cost ratio. 

The advancing front of gypsy moth infestation is now located in the states of Michigan, Ohio, 

West Virginia, Virginia, and North Carolina. Any further advances into the next tier of states will 

greatly increase the cost of control and magnify proportionally the area from which artificial 

introductions can emanate. The 1952 appraisal documented that between 50 and 80 percent of the 

forest land in the states of Ohio, Tennessee, Kentucky, and Missouri was classified as susceptible to 

gypsy moth damage, based on proportion of favored food species, dry sites, poor stocking, and a history 

of land abuse. Clearly, there is much at risk beyond the advancing front. 

A meeting of state and federal officials was recently held in Raleigh, North Carolina, to discuss 

the feasibility of containment given available technology and current distribution of the insect. A series 

of recommendations was drafted, one of which states that "a comprehensive research, development, 

operational plan should be developed that is specifically designed to culminate in a containment trial." 

The group concluded that containment is a potentially viable management strategy because of the 

limited mobility of the insect and because of the existence of a number of technologies that could be 

utilized in a containment program. 

In essence, a containment program already exists. In 1988, the Appalachian Integrated Pest 

Management Program (AIPM) was implemented in a 38-county area of Virginia and West Virginia 

encompassing 5.2 million ha. One of the stated goals of this project is to minimize the spread of the 

gypsy moth through the AIPM area. A 2-3 km grid of pheromone traps is used to monitor 

populations throughout the project area. Data from these traps provide a measure of the distribution 

of the gypsy moth and identify areas where more intensive surveys are needed to detect possible 

outbreaks. Control tactics can then be deployed against spot infestations before they expand and cause 

economic damage. Treatments in the designated "transition zone" (Fig. 1) are analogous to the tactics 

used in the barrier zone in New England, though the pheromone traps now being used are far superior 

to the labor intensive practices used earlier. Furthermore, whereas treatments in the barrier zone 

consisted of creosoting egg masses and ground spraying with lead arsenate (neither of which is 

183 
environmentally acceptable), we now have at our disposal biological and chemical pesticides, sterile 

insects, and pheromone technology that are environmentally acceptable by today's standards. 

For those who may be skeptical that biological pesticides alone can eradicate an established 

infestation, three aerial applications of Bt coupled with intensive pheromone trapping to delineate 

residual populations were successful in eliminating the large infestation in Oregon over a 3-year period 

beginning in 1984. The area requiring treatment declined from 225,000 a in 1985, to 190,000 a in 

1986, and to 12,000 a in 1987, when only 40 male moths were trapped. By expanding the existing 

AIPM pheromone trap network in Virginia and West Virginia through North Carolina to the east and 

through Ohio to the west, we could establish a containment zone within which gypsy moth populations 

could be delineated and suppressed as deemed necessary. 

Perhaps the greatest deterrent to a containment strategy is the lack of a concerted federal 

commitment. At present, the Animal and Plant Health Inspection Service (APHIS) maintains the 

federal regulatory quarantine mainly by regulating the shipment of household goods out of the infested 

region and by detecting and eliminating isolated infestations, but funding for APHIS programs has not 

kept pace with inflation and their success has been compromised. APHIS programs must be continued 

and strengthened. As argued in the Ketron report, an effective containment strategy must be 

implemented to eliminate all artificial spread and eliminate natural spread. There must also be a 

federal commitment to provide the funds needed to suppress gypsy moth populations along the 

advancing front when densities exceed a threshold level. This is lacking in the current federal policy 

providing states only with matching funds. During actual outbreaks, funds available to the states are 

sufficient to treat only the highest priority forested lands. 

To offset the high cost of containment, states in the second and third tiers beyond the advancing 

front should contribute to the effort as an investment in the future. A projected cost of $10 million 

per year is much more affordable when divided between 12 or more states as opposed to the five that 

make up the advancing front. 

In the final analysis, if the costs are not prohibitive, the technology is adequate, and a shared 

state and federal commitment is made, there is every reason to believe that a containment program to 

slow the spread of the gypsy moth can be successful. Moreover, if we maintain the gypsy moth status 

quo for 5 to 10 years, there is a good possibility that ongoing bio-technological research will provide 

us with more effective tools for coping with the gypsy moth problem. 

LITERATURE CITED 

BARBOSA, P., WALDVOGEL, M., and MARTINAT, P. 1983. Developmental and reproductive 

performance of the gypsy moth, Lymantria dispar (L.) (Lepidoptera: Lymantriidae ), on selected 

hosts common to mid-Atlantic and southern forests. Environ. Entomol. 12: 1858-1862. 

BARBOSA, P., MARTINAT, P., and WALDVOGEL, M. 1986. Development, fecundity, and survival of 

the herbivore Lymantria dispar and the number of plant species in its diet. Ecol. Entomol. 

11: 1-6. 

BESS, H.A, SPURR, S.H., and LITTLEFIELD, E.W. 1947. Forest site conditions and the gypsy moth. 

Harv. For. Bull. 22. 

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containment. Report KFR 161-78. Ketron, Inc., Arlington, Virginia. 65 p. 

BROWN, R.C. and SHEALS, R.A 1944. The present outlook on the gypsy moth problem. J. For. 

42: 393-407. 

184 
CAMPBELL, R.W. and SLOAN, R.J. 1977. Forest stand responses to defoliation by the gypsy moth. 

For. Sci. Monogr. 19. 34 p. 

COLLINS, C.W. 1917. Methods used in determining wind dispersion of the gypsy moth and some other 

insects. J. Econ. Entomol. 27: 170-177. 

FELT, E.P. 1942. The gypsy moth threat in the United States. Eastern Plant Board Circular No. 1. 

16 p. 

FOSBERG, M.A and RELING, D. 1986. Modeling airborne transport of gypsy moth (Lepidoptera: 

Lymantriidae) larvae. Agric. For. Methodol. 38: 1-8. 

GANSNER, D.A and HERRICK, O.W. 1985. Host preferences of gypsy moth on a new frontier of 

infestation. U.S. Dep. Agric. For. Serv. Res. Note NE-330. 

GANSNER, D.A, HERRICK, O.W., DEBOLD, P.S., and ACCIAVATTI, R.E. 1983. Changes in forest 

condition associated with gypsy moth. J. For. 81: 155-157. 

GIESE, R.L. and SCHNEIDER, M.L. 1979. Cartographic comparisons of Eurasian gypsy moth 

distribution, Lymantria dispar L. (Lepidoptera: Lymantriidae). Entomol. News 90: 1-16. 

GOTTSCHALK, K. W. and TWERY, M.J. 1989. Gypsy moth impacts in pine-hardwood mixtures, 

p. 50-58. In Proc. Pine-hardwood mixtures: a symposium on management and ecology of the 

type. 18-19 April 1989, Atlanta, Georgia. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. SE-58. 

271 p. 

HERRICK, O.W. and GANSNER, D.A 1986. Rating forest stands for gypsy moth defoliation. 

U.S. Dep. Agric. For. Serv. Res. Pap. NE-583. 4 p. 

HERRICK, O.W. and GANSNER, D.A 1988. Changes in forest condition associated with gypsy moth 

on new frontier of infestation. North. J. Appl. For. 5: 59-61. 

HICKS, R.R. and FOSBROKE, D.E. 1987. Stand vulnerability: can gypsy moth damage be predicted? 

p. 73-80. In Coping with the Gypsy Moth in the New Frontier: A Workshop for Forest 

Managers. 1987. West Virginia Univ. Books, Morgantown, WV. 153 p. 

HOUSTON, D.R. and VALENTINE, H.T. 1977. Comparing and predicting forest stand susceptibility to 

gypsy moth. Can. J. For. Res. 7: 447-461. 

KEGG, J.D. 1973. Oak mortality caused by repeated gypsy moth defoliation in New Jersey. J. Econ. 

Entomol. 66: 639-641. 

KORSTIAN, C.F. and RUGGLES, AG. 1941. Report of findings and recommendations with references 

to the gypsy moth project of the Bureau of Entomology and Plant Quarantine. J. For. 

39: 973-979. 

LECHOWICZ, M.J. and MAUFFETTE, Y. 1986. Host preferences of the gypsy moth in eastern North 

America versus European forests. Rev. Entomol. Queb. 31: 43-51. 

MADRID, F.J. and STEW ART, R.K. 1981. Ecological significance of cold-hardiness and winter 

mortality of eggs of the gypsy moth, Lymantria dispar L., in Quebec. Environ. Entomol. 

10: 586-589. 

185 
MASON, C.J. and McMANUS, M.L 1981. Population dynami~, p. 65-216. In Doane, C.C. and 

McManus, M.L, eds. The Gypsy Moth: Research Toward Integrated Pest Management. 

U.S. Dep. Agric. For. Serv. Tech. Bull. 1584. 757 p. 

MASON, G.N. 1987. Rating stand susceptibility to gypsy moth defoliation, p. 65-72. In Coping with the 

Gypsy Moth in the New Frontier: A Workshop for Forest Managers. West Virginia Univ. 

Books, Morgantown, W. VA 153 p. 

MILLER, C.A 1958. The measurement of spruce budworm populations and mortality during the first 

and second larval instars. Can. J. Zool. 36: 409-422. 

MILLER, J.C. and HANSON, P.E. 1989. Laboratory studies on development of gypsy moth, Lymantria 

dispar (L) (Lepidoptera: Lymantriidae ), larvae on foliage of gymnosperms. Can. En to mol. 

121: 425-429. 

MONTGOMERY, M.E., McMANUS, M.L, and BERISFORD, C.W. 1989. The gypsy moth in pitch 

pine-hardwood mixtures: predictions for the South based on experiences in the North, p. 43-49. 

In Proc. Pine-hardwood mixtures: a symposium on management and ecology of the type. 

18-19 April 1989, Atlanta, Georgia. U.S. Dep. of Agric., For. Serv. Gen. Tech. Rep. SE-58. 

271 p. 

MOSHER, F.H. 1915. Food plants of the gypsy moth in America. U.S. Dep. Agric. Tech. Bull. 250. 

39 p. 

PERRY, C.C. 1955. Gypsy moth appraisal program and proposed plan to prevent spread of the moths. 

U.S. Dep. Agric. Tech. Bull. 1124. 27 p. 

QUIMBY, J.W. 1987. Impact of gypsy moth defoliation on forest stands, p. 21-29. In Coping with the 

Gypsy Moth in the New Frontier: A Workshop for Forest Managers. West Virginia Univ. 

Books, Morgantown, W. VA 153 p. 

TAYLOR, R.AJ. and RELING, D. 1986. Density/height profile and long-range dispersal of first-instar 

gypsy moth (Lepidoptera: Lymantriidae ). Environ. Entomol. 15: 432-435. 

VALENTINE, H.T. and HOUSTON, D.R. 1984. Identifying mixed oak stand susceptibility to gypsy 

moth defoliation: an update. For. Serv. 30: 270-271. 

186 
INTEGRATING HOST, NATURAL ENEMY, AND 

OTHER PROCESSES IN POPULATION MODELS 

OF THE PINE SAWFLY 

AA SHAROV 

Entomology Department, Moscow State University 

Lenin Hills, Moscow 119899 U.S.S.R. 

INTRODUCTION 

Explanation of population dynamics is one of the main problems in population ecology. There 

are two main approaches to the explanation: the factor approach and the dynamic approach. 

According to the first, an explanation is obtained when the effect of various environmental factors on 

population density is revealed. Such analysis is performed using well developed regression methods 

(Poole 1978). The resulting regression equations can be used for prediction of population density and 

their coefficients indicate the role of each factor in population change. This method of explanation 

considers the population as a black box with inputs and outputs. Population predictions obtained by 

regression are relevant only for stationary systems and only if mechanisms of population dynamics do 

not change. 

The dynamic approach is oriented to the analysis of mechanisms of population change. It can 

predict the consequences of deliberate change of these mechanisms and, thus, it is more useful for 

population management than the factor approach. The dynamic approach deals with a system 

consisting of a population and its environment, a life system (Oark 1964). When applying the dynamic 

approach one must distinguish between factors and processes. A factor is a characteristic of the life 

system state. Clark et al. (1967) used the term "codeterminant" instead of "factor." But I prefer the 

term "factor" because its has became traditional in ecology. A process is a flow of similar ecological 

events that are taking place in a life system. Reproduction, mortality, growth, development, and 

migration are examples of ecological processes. There exist different mortality processes in each 

population. These processes correspond to different developmental stages of dying organisms and to 

different causes of mortality. For example, spontaneous larval and pupal mortality of a certain insect 

are different processes. Also, population decreases caused by predation and parasitism are the result of 

two different processes. 

Life tables are widely used for the analysis of mortality in animal populations (Harcourt 1969, 

Varley et al. 1973). In these tables, mortality processes are termed as "mortality factors." This term is 

quite ambiguous because it includes both death processes and the factors affecting the rate of this 

process (Sharov 1985). But factors and processes cannot be identified for two reasons. First, there is 

no one-to-one correspondences between them. For example, insect mortality caused by predation 

depends not only on predator density but also on prey density, refuge capacity, temperature, and other 

factors as well. Temperature is a factor affecting the rates of many other processes: growth, 

reproduction, migration, and so on. Second, factors which influence the process rates may interact so 

that mortality levels cannot be attributed to individual factors. Thus, we reject the term "mortality 

factor." 

BARANCHIKOV, Y.N., MATrSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

187 
A life system can be described formally by a simulation model which uses the information about 

factor influence on process rates and factor change in the course of ecological processes. Simulation 

models are considered to be the basis for scientific explanation of population dynamics (Clark et al. 

1967, Berryman 1981). But the behavior of a simulation model is often difficult to explain like the 

behavior of a real population. 

Therefore, in practice the explanation of population dynamics is usually based not on simulation 

models but the statistical analysis of life tables. Using k-factor analysis one can reveal key mortality 

factors (Varley and Gradwell 1960, Podoler and Rogers 1975). Regression methods allow us to 

distinguish density-dependent factors which are believed to play a regulative role in population 

dynamics (Morris 1959, Varley et al. 1973). These methods have two main drawbacks. First, they use 

the term "mortality factor" which, as has been shown, leads to wrong interpretation. For example, 

temperature and humidity are usually not given in life tables and, therefore, they cannot be key factors 

despite their strong effect on population. Second, traditional methods of life table analysis do not 

provide us with sufficient information about life system structure. For example, the regulative role of 

ecological process in population dynamics is evaluated on the base of its density dependence, while 

ignoring its interaction with other processes. The possibility that density regulation is performed by 

process interaction is not taken into account. Thus it is not surprising that in many relatively stable 

populations, density dependent factor have not been revealed (Dempster 1983). The fact that some 

mortality factor is a key or density dependent one tells nothing about what will happen after its 

deliberate change. 

Thus the dynamic approach, in spite of its advantages as compared with the factorial one, does 

not provide methods for evaluating factors and processes in population dynamics. 

In this work I attempt to evaluate the role of factors and processes depending on their 

contribution to quantitative characteristics of population dynamics. This method allows us to reveal 

the role of process interactions. 

Two approaches (empirical and simulational) can be applied in the analysis of the role of factors 

and processes in population dynamics. Using the empirical approach one should change factor values 

or process trends in the real life system and then consider the response of quantitative characteristics 

of population dynamics. In the simulational approach such experiments are simulated by a computer 

mathematical model. The latter approach is less expensive. Moreover, it is possible to simulate such 

changes of the life system that are not possible or not desirable in practice. However, the simulational 

approach is indirect, its precision depends on the validity of a simulation model. In this work we use 

the simulation approach. 

The proposed method of a population analysis is applied to the common pine sawfly, Diprion 

pini L, a dangerous pest of pine plantations. It overwinters as an eo nymph (prepupa) in cocoons in 

the litter or the upper soil layers. Eonymphs having visible rudimentary pupal eyes are called 

pronymphs. There are 2 to 34 percent pronymphs among hibernating sawflies (Avramenko 1970). 

Overwintered sawflies have two flight periods: late April to early May and late July to early August 

(Sharov and Safonkin 1982). Sawflies hibernated as pronymphs emerge in both periods (about 

60 percent in the first period and about 40 percent in the second period), while sawflies hibernated as 

eo nymphs emerge only in the second period (about 35 percent). The remaining eonymphs maintain 

their diapause during the next whole year or longer. 

Female sawflies oviposit into a split made along the edge of the pine needle. Eggs laid by one 

female usually occupy a needle cluster (Dusaussoy and Geri 1966). Larvae hatched from an egg cluster 

form a colony. In July eonymphs make cocoons in pine crowns and from September to October in the 

litter and soil. Emergence of sawflies from summer cocoons nearly coincides in time with the second 

flight period of the overwintered generation. Thus in August there are larvae of the first and second 

generations. To avoid confusion, we use the term "wave of development" instead of "generation." 

188 
Sawflies developing in May to June belong to the first wave of development, and the sawflies 

developing from August to October belong to the second wave. In the Rostov region the common 

pine sawfly has outbreaks of mass reproduction within 3 to 6 years (Kharlashina 1984). Outbreaks 

usually follow those years with hot, dry summers. 

METHODS 

Simulation Modelling 

The model proposed in this paper is based on our previously published data on the life cycles 

and survival of the common pine sawfly and its parasitoids (Sharov 1982, 1983, 1986b, 1987, 1988, 

Sharov and Safonkin 1982). Principles of modelling were adopted from the model of winter moth 

(Varley et al. 1973). The mean temperature in May to September is an input variable. Parameters of 

the model were partially taken from experimental data and partially found by the maximum likelihood 

procedure. The model validity was evaluated on a qualitative level by its ability to predict pest 

outbreaks. Information about sawfly outbreaks in the Rostov region (Kharlashina 1984) and 

temperature from 1956 to 1983 were used as a test. 

Quantitative Characteristics of Sawfly Population Dynamics 

Sawfly population dynamics as a whole was characterized by the mean level and standard 

deviation- of a log-transformed (natural logs) late-ins tar larvae density in the second wave of 

development. Pest density in the first wave of development has not been considered because it was 

smaller than the density in the second wave. Log-transformation is necessary because of a log-normal 

distribution of population density. Mentioned characteristics were estimated using the simulation of a 

population dynamics. The real mean temperature from May to September during the 28-year-period 

from 1956 to 1983 was taken as an input variable. 

The population dynamics pattern of the common pine sawfly is complex because of repeated 

outbreaks of the pest. We analyzed each period of an outbreak separately. Isaev and Khlebopros 

(1974) distinguished five periods in the phase portrait of an outbreak cycle of forest insect pests: 

period of stability, increase, maximum, collapse, and depression. The common pine sawfly has a very 

short period of maximum, and thus we considered only the other four periods. 

The period of stability is characterized by coefficients of m- and v-stability (in previous 

publications (Sharov 1986a) they were called coefficients of buffering and homeostasis, respectively), 

describing different aspects of population density regulation. They were estimated using the simulation 

model with the mean temperature from May to September being constant and equal to 18.6°C, which 

is the average temperature in non-drought years. Let x be the mean log-transformed late-instar larvae 

density in the second wave of development and z--the mean log-transformed larvae survival in the 

same wave of development before the measurement of population density. In both cases, averaging was 

performed across a number of years. If the value z becomes lower due to additional mortality, the 

value x decreases. The coefficient of m-stability is defined as 

It indicates how difficult it is to suppress the population density. The greater its value, the more 

additional mortality is needed for population suppression. 

(1) 

Another important aspect of population regulation is the v-stability, which prevents the increase 

of the amplitude of density fluctuations. It is described by the coefficient of v-stability: 

189 
VS = (ds2x/ds2z)-l 

where s 2 x and s2 z are variances of the log-transformed sawfly larvae density, x, and the 

log-transformed survival, z . When s2 z is infinitesimal and the system is in a stable state, then: 

VS = s2 ;s2 Z X 

(2) 

(3) 

The rate of an increase of sawfly density at the beginning of the outbreak is characterized by the 

index ln£N0 jN 8 ), where N 8 and N0 are late-ins tar larval densities in the second wave of development 

per 1 m in the period of stability and during the outbreak, correspondingly. The rate of density 

decrease at the period of population collapse is characterized by the index ln(N0 /Nc), where Nc is the 

larval density after an outbreak. 

Rates of population density fluctuation were estimated using the simulation model. We assumed 

that the mean temperature from May to September was 18.6°C and it did not change from year to year 

(the period of stability); then it increased up to 21.fOC for only one year (the simulation of a drought) 

and after that it was stable at the initial level. The density N 8 was measured in the year before the 

drought, N0 in the next year after drought and Nc in the second year after drought. 

In a period of depression of a sawfly population, drought generally does not cause repeated 

outbreak; if it does, outbreak is less intensive. This property is characterized by the coefficient of 

"refractoriness" 

4 

R = ~ ln(N0 /Ni) 

i=2 (4) 

where N0 is the larval density in the next year after the first drought and N 1 is the same density in the 

next year after the second drought which happens i years after the first drought. For i more than 4 

the refractory effect is lost. The coefficient R was estimated using the simulation model. The drought 

was simulated by rising the mean May to .September temperature from 18.6°C to 21.1 °C. 

Confidence limits for all quantitative characteristics estimated using the simulation model were 

found by the following method: a set of versions of the initial model was obtained by independent 

stochastic variation of the 32 most important parameters of the model. Standard deviations of these 

parameters were equaled to their standard errors. For selection of adequate model versions the 

population dynamics was simulated assuming the droughts occurred periodically every 4 years. Then 

the estimated parasitization rate of sawfly eggs and eonymphs was compared with our empirical data 

obtained from 1977 to 1979. As a result 10 model versions, including the initial one, were selected for 

simulation of the dynamics of the sawfly's parasitization rate. 

Each quantitative characteristic was estimated using all 10 model versions and then the mean 

value, standard deviation "s" (in this case it is taken as standard error) and half of the confidence 

interval "ts" ("t" is the student's criterion for P = 0.05) were found for each characteristic. In the 

following text half of the confidence interval is given after the signs "+ ". 

Analysis of Process and Factor Contributions to the Quantitative 

Characteristics of Population Dynamics 

The contribution of individual processes and their interactions to the quantitative characteristic 

y 1 of population dynamics was evaluated using the equation: 

(5) 

190 
where v j is an integer variable indicating the dependence of the j-th ecological process on factors, and 

.&_1 is the coefficient representing the contribution of the j-th ecological process or process interaction 

(if the coefficient has more than one index) to the value y 1. The variable v_1 has only two meanings: 

v j = 1 if the rate of j-th process naturally depends on factors and v j = 0 if this rate is fixed at the 

equilibrium level peculiar to the period of stability. Process rates were fixed only in that period of an 

outbreak cycle, in which we wanted to examine the role of these processes. The value y i was 

estimated using the model with different combinations of processes having the fixed rate. Then 

coefficients &j were obtained by the multi-factor regression technique (Maximov 1980). 

The "refractoriness" of the sawfly population is associated with a special postoutbreak state of 

the life system. We analyzed what factors peculiar for this state gave the greatest contribution to the 

coefficient of refractoriness R. In the course of simulation the value of different factors was changed 

in winter following the outbreak of the sawfly population. Values peculiar to the period of stability 

were given to these factors. The refractory role of factors was evaluated by the response of the 

coefficient of refractoriness to factor change. 

The role of parasitoids in sawfly population dynamics was examined by simulation of their 

exclusion from the life system. The change of the mean value and standard deviation of the 

log-transformed sawfly larvae density was analyzed. 

RESULTS 

Simulation Model 

The proposed model simulates the multiple year dynamics of the common pine sawfly 

population. It has been described in detail (Sharov 1986b). A year is the basic time unit. There are 

four blocks describing the sawfly population, its host tree Pinus sylvestris L., and two groups of 

parasitoids developing in sawfly eggs and eonymphs. The model describes the change of population 

density of the sawfly and its parasitoids in their life-cycle and the dynamics of the amount of needles 

on the pine trees. Sawfly mortality caused by parasitoids was described by the modified model of 

Rogers (1972). In this model I assumed that the area of discovery (a) depends on the parasitoid 

density (P) in accordance with the model of Hassell and Varley (1969): a = Q P -m, where Q and m 

were parameters. Sawfly-host plant interaction was described by the model of Semevski (1971). 

According to this model the pest space distribution is log-normal. The number of surviving larvae on 

each tree was assumed to be equal to the number of food units on the tree. If food is in plenty there 

is no mortality due to food shortage. The initial distribution of needles on trees was assumed to be 

uniform. 

Sawfly fecundity is constant. Young larval survival increases with the size of a colony, the group 

effect (Sharov 1988). The size of a colony, in tum, depends on egg mortality due to parasitism. 

Last-instar larval and eonymph mortality was assumed to depend on mortality caused by food shortage 

and on mean May to September temperature in the previous and current years. The effect of 

temperature on larval mortality in the model is an explication of the effect of host-plant quality, 

dependent on weather. It is known that pine tree weakening caused by water deficiency is usually 

associated with high temperature and favors sawfly development (Schwenke 1964, Kharlashina 1984 ). 

Reactivation of diapausing sawfly eonymphs depends on temperature in a dose-effect manner. 

The temperature increases the reactivation rate in the second flight period of the current year and the 

first flight period in the next year (Sharov and Safonkin 1982). The reactivation rate in the first flight 

period is considerably reduced after an outbreak. In the model it depends on sawfly larvae density in 

the previous year. 

191 
The model appeared to be adequate at the qualitative level. It "predicted" five out of six sawfly 

outbreaks in the Rostov region from 1956 to 1983 (Sharov 1986b ). It is important that this model not 

only predicts pest outbreaks (they can be predicted by a simple regression model as well), but that it 

also describes mechanisms of a population alteration. It shows that its basic assumptions are sufficient 

for simulation of the high rate of sawfly density increase at the beginning of an outbreak. 

Role of Processes and Factors in Population Dynamics 

The role of six ecological processes in the dynamics of the common pine sawfly population was 

examined: 1) egg mortality caused by parasitoids, 2) eonymphs mortality caused by parasitoids, 

3) larval mortality caused by food shortage, 4) sawfly reactivation in the first flight period, 5) sawfly 

reactivation in the second flight period, and 6) larval mortality caused by diseases. 

In the period of stability the coefficients of m- and v-stability of the sawfly population appeared 

to be MS = 0.70 + 0.12, VS = 0.30 + 0.19. Population m- and v-stability are linked mainly with the 

interaction of the sawfly with the parasitoids (Table 1 ). Parasitoids of eggs and eonymphs give an 

approximately equal contribution to the coefficient of m-stability in the sawfly life system (.&1 = 0.51, 

&2 = 0.41). Eonymph parasitoids give the greater contribution to the coefficient of v-stability of the 

host &2 = 0.68) than egg parasitoids (&1 = 0.20). Interaction of mortality processes associated with 

two groups of parasitoids destabilizes the sawfly population dynamics (.&12 = -0.59). 

The model predicts the high rate of sawfly density increase after drought. In a dry year the 

late-instar larval density in the second wave of development becomes 101 + 36 m- 2 as compared with 

34 + 11 m- 2 in the period of stability. In the next year it increases to 995 + 368 m- 2. The 

reduction in larval mortality caused by diseases after drought when host plants are weakened is most 

important in population density increase ( .&6 = 0.55) (Table 1 ). Mass reactivation of sawflies in the 

first flight period is also important (&4 = 0.35). 

The sum of regression coefficients (5) for process interactions (2.32) is much greater than that 

for individual processes (1.05). Thus, process interactions but not individual ones play an important 

role in the increase of sawfly density at the beginning of an outbreak. The most important are 

interactions of temperature-dependent processes (No. 4-6) with that of egg mortality caused by 

parasitoids (&16 = 0.46, &15 = 0.37, &14 = 0.32). 

The period of density increase is naturally followed by the period of collapse. According to the 

simulation, in the first year after the outbreak, sawfly larval density becomes approximately only onethird as large as in the period of stability. The larval mortality caused by food shortage plays the 

dominant role in the fall of population density (.&3 = 1.61). The sum of regression coefficients for 

process interactions (2.02) is greater than that for individual ones (1.92). This indicates the 

importance of process interactions in the sawfly density increase. The interaction of larval mortality 

caused by food shortage with that of eggs caused by parasitism is particularly important (.&13 = 1.75). 

If food is in plenty, parasitoids cannot suppress the sawfly population (.&1 = -0.83, .&2 = 0.69). 

Eonymph parasitoids cannot decrease the host density even in conditions of food shortage (coefficient 

&23 is non-significant). 

In the period of depression, the life system of the common pine sawfly is characterized by a 

decrease in density of "new" eonymphs diapausing less than 1 year, increased density of "old" eonymphs 

with diapause period more than 1 year, elevated density of parasitoids, and decreased amount of needle 

as compared with the period of stability. After the change of 1) "new" eonymph density, 2) "old" 

eonymph density, 3) amount of needle in trees, 4) density of egg parasitoids, and 5) density of 

eonymph parasitoids to the value peculiar for the stability period, the coefficient of refractoriness 

192 
Table 1. Effect of ecological processes on quantitative characteristics of 

the common pine sawfly Diprion pini L. population dynamics. 

.& coefficients Quantitative characteristics of population dynamics ** 

of equation 

(5)* Y1 = MS Y2 = VS Y3 = ln(No/Ns) Y4 = ln(No/Nc) 

0 0 0 0 0.62 ± 0.15 

1 0.51 ± 0.17 0.20 ± 020 0 -0.83 ± 0.38 

2 0.41 ± 0.11 0.68 ± 0.09 0 0.68 ± 0.26 

12 -0.22 ± 0.10 -0.59 ± 0.10 0 0.54 ± 0.35 

3 -0.01 ± 0.01 -0.02 ± 0.01 0 1.61 ± 0.50 

13 0.01 ± 0.01 0.02 ± 0.01 0 1.75 ± 0.52 

23 0.01 ± 0.01 0.02 ± 0.01 0 -0.15 ± 0.20 

123 -0.01 ± 0.01 -0.02 ± 0.01 0 0.51 ± 0.52 

4 0 0 0.35 ± 0.12 0.45 ± 0.15 

14 0 0.01 ± 0.01 0.32 ± 0.11 0.12 ± 0.16 

24 0 0 0.05 ± 0.03 -0.34 ± 0.15 

124 0 0 0.05 ± 0.03 -0.28 ± 0.16 

34 0.01 ± 0.01 0.02 ± 0.01 0 -0.36 ± 0.11 

134 -0.01 ± 0.01 -0.02 ± 0.01 0 -0.35 ± 0.19 

234 -0.01 ± 0.01 -0.02 ± 0.01 0 0.26 ± 0.12 

1234 0.01 ± 0.01 0.02 ± 0.01 0 0.33 ± 0.26 

5 0 0 0.15 ± 0.09 0 

15 0 0 0.37 ± 0.27 0 

45 0 0 0.13 ± 0.04 0 

145 0 0 0.17 ± 0.12 0 

6 0 0 0.55 ± 0.15 0 

16 0 0 0.46 ± 0.15 0 

46 0 0 0.24 ± 0.07 0 

146 0 0 0.13 ± 0.12 0 

56 0 0 0.20 ± 0.05 0 

156 0 0 0.29 ± 0.16 0 

456 0 0 -0.05 ± 0.02 0 

1456 0 0 -0.22 ± 0.07 0 

Sum of the 0 0 0.18 ± 0.14 0 

coefficients 

Total 0.70 ± 0.12 0.30 ± 0.19 3.37 ± 0.45 4.56 ± 1.08 

* Numbers of ecological processes: 1) egg mortality due to parasitoids, 

2) eonymph mortality due to parasitoids, 3) larval mortality due to food 

shortage, 4) sawfly reactivation in the first flight period, 5) sawfly 

reactivation in the second flight period, and 6) larval mortality due to 

diseases. 

** MS and VS are coefficients of m- and v-stability of the sawfly population 

in the period of stability; N8 , N0 and Nc are population densities of sawfly 

larvae per 1 m2 in the second wave of development in the period of stability, 

outbreak and collapse, correspondingly. 

193 
appeared to be 1) 8.0 + 3.4, 2) 8.5 + 2.6, 3) 6.8 + 4.2, 4) 6.8 + 2.0, 5) 1.2 + 1.6, correspondingly. 

In the control where no factor was deliberately changed, the coefficient of refractoriness was equal to 

7.5 + 3.5. Thus the refractoriness of the sawfly life system in the period of depression is associated 

with the elevated density of eonymph parasitoids. The other factors including density of egg parasitoids 

and amount of needles in the trees has no refractory effect. 

According to the simulation, the exclusion of each group of parasitoids from the life system of 

the host leads to an increase of the mean log-transformed sawfly density (Table 2). Egg parasitoids 

suppress the mean host density to a greater extent than parasitoids of eonymphs. The standard 

deviation of log-transformed sawfly density decreased significantly after the exclusion of egg parasitoids. 

This fact indicates the destabilizing role of the parasitoids in population dynamics of their host. 

DISCUSSION 

Mechanisms of common pine sawfly population dynamics in the Rostov region are similar to 

those in western Europe (Dusaussoy and Geri 1966, Eichhorn 1977, 1982, Geri and Goussard 1984). 

Nevertheless there are some differences. The primary one is connected with the mechanisms of 

reactivation of overwintered sawflies. There are three flight periods of the common pine sawfly in 

western Europe instead of just two as in the Rostov region. The additional flight period takes place 

in July and is often the most intensive one. 

In France outbreaks of mass reproduction of the sawfly have been recorded at time intervals of 

17 to 28 years (Geri and Goussard 1984), less often as compared with the Rostov region where the 

average time interval between outbreaks is 4 years (Kharlashina 1984). This outbreak pattern is 

common in all geographical regions. The provoking event is apparently drought that weakens a host 

plant and thus increases sawfly survival. The reactivation rate of the pest also increases, particularly in 

the first flight period in the year following drought. As a result, the seasonal cycle of the pest 

becomes mainly bivoltine instead of monovoltine in the stability period. Consequently, the population 

growth rate increases. The parasitization rate of the sawfly decreases, which might be interpreted as 

the escape from parasitoids. In the period of a population decline the parasitization rate increases 

greatly up to 100 percent (Urban 1962, Eichhorn 1982, Kristek and Petruska 1982). Mortality caused 

by diseases and proportion of diapausing sawflies increase as well. In some cases lowered fertility has 

been observed (Urban 1962, Eichhorn 1982, Geri et al. 1990). After the outbreak the rate of 

parasitism decreases gradually. In the Rostov region we have observed all these effects except the 

lowered sawfly fertility at the end of an outbreak (Sharov 1982, 1986b, 1987). 

But enumeration of peculiarities of different outbreak periods does not explain a population 

alteration. It is necessary to prove that a given set of phenomena considered is enough for adequate 

outbreak simulation, and to evaluate quantitatively the role of each ecological process in a population 

dynamics. It has not been done before. 

Known mechanisms of common pine sawfly population dynamics do not allow us to explain its 

fast population growth at the beginning of an outbreak. According to Kharlashina (1984), larval 

mortality caused by disease, host tree resistance, and other factors comprises not more than 30 percent 

of the total mortality. If the mortality level from drought-induced host plant weakening were three 

times lower, the sawfly density would be 1.29 times higher in 1 year. Taking into account 

transformation of the seasonal cycle from monovoltine to bivoltine, the pest density might be 1.292 = 

1.65 times as high. Such a density alteration is too small to escape parasitoids. When considering the 

effect of parasitism, one can explain a two- to threefold increase in sawfly density, but natural 

population density rises two orders of magnitude during an outbreak. 

194 
Table 2. Consequences of parasitoid exclusion from the life system of the 

common pine sawfly (based on data simulation) 

Mean log-trans- Standard deviation 

formed sawfly of log-transformed 

Presence Presence of larvae density sawfly larvae denof egg eo nymph in the second wave sity in the second 

parasitoids parasitoids of development wave of development 

Yes Yes 3.85 ± 0.20 1.53 ± 0.24 

Yes No 4.62 ± 0.27 1.36 ± 0.34 

No Yes 5.66 ± 0.39 0.46 ± 0.12 

No No 5.94 ± 0.36 0.40 ± 0.05 

There are no explanations for the increased rate of parasitism during population collapse. 

Elevated parasitoid performance can be associated with their increased density. But in this explanation 

the greater population growth rate of the sawflies compared to that of parasitoids has not been taken 

into account. Thus the parasitism rate can only grow if some other factors inhibit the growth of the 

host population. 

Analysis of the role of an ecological process in the alteration of a sawfly population helps 

explain the phenomenon. Previous attempts to explain the pattern of sawfly population dynamics failed 

because the interaction of ecological processes were taken into account. We have revealed the 

dominant role of the process interactions in the course of a sawfly outbreak. Simulation modelling is 

the only correct method for the description of process interactions. Thus an explanation of population 

dynamics can be obtained only by this method. 

Some mechanisms previously not taken into account were included in our model. For example, 

we found that the rate of eonymph reactivation in the second flight period increased with temperature 

(Sharov and Safonkin 1982). The model showed this as an important mechanism of the sawfly density 

increase after drought. 

Table 1 indicates escape of the sawfly population from parasitoids at the beginning of an 

outbreak as an interaction of temperature dependent processes (No. 4-6) with an egg mortality caused 

by parasitoids. In the collapse period parasitoids do not play any important role, but their interaction 

with larval mortality caused by food shortage is important. This interaction is interpreted as follows: 

sawflies increase their density until food exhaustion, and then parasitoids have the time to outnumber 

their host and to suppress the host population. Unlike eonymph parasitoids, egg parasitoids are more 

important in host suppression because their interaction with the sawfly occurs in an earlier phase of 

the life cycle. When the number of host eggs is sufficiently reduced by egg parasitoids, some hosts are 

available for eonymph parasitoids. 

In the depression period, repeated drought does not provoke an extra outbreak because the 

increased density of eonymph parasitoids controls the population number of their host. Approximately 

3 years after an outbreak the parasitism rate of the sawfly eonymph decreases. The next drought, in 

turn, will cause a new outbreak of the pest. After an outbreak, the density of egg parasitoids 

decreases faster compared to parasitoids of the eonymphs. This is due to the absence of a prolonged 

diapause in egg parasitoids. Thus they are not able to support refractoriness of the sawfly life system. 

195 
In the period of stability, the sawfly population is regulated by parasitoids. Both groups of 

parasitoids prevent the mean density alteration of the host, however only the eonymph parasitoids 

stabilize host density fluctuations. These regulation mechanisms are rather weak and cannot maintain 

population density at the equilibrium level during drought. Consequently another outbreak will begin. 

In general, an outbreak pattern of sawfly population dynamics is determined primarily by egg 

parasitoids. On the one hand, they are not able to maintain a low host density under unstable weather 

conditions; on the other hand, they prevent continuation of a high pest density during an outbreak. 

Eonymph parasitoids maintain the refractoriness of a sawfly life system after an outbreak and play a 

certain role in the "escape effect" during host density increase. 

These conclusions are supported by the simulation experiment with parasitoid exclusion. Sawfly 

outbreaks do not occur without egg parasitoids, however, the mean sawfly density increases. Thus egg 

parasitoids suppress and destabilize the host population. Similar parasitoid effects on host insect 

population dynamics was reported earlier for Prieria sinica Moore (Shiotsu and Tsubaki 1986) and for 

Epinotia tedella Gl. (Munster-Swendesen 1985). 

Thus the proposed method for explanation of population dynamics pattern allows us to describe 

quantitatively the role of factors and processes in the common pine sawfly life system. The process 

interaction was shown to play the dominant role in the course of an outbreak of the pest. This fact is 

evident through the "entirety" of the life system and shows the necessity of the system's approach to 

life system analysis. 

SUMMARY 

The role of ecological factors and processes in the population dynamics of the common pine 

sawfly, Diprion pini L., was examined using a simulation model. Consequences of fixation of densityand temperature-dependent process rates were determined. Results were processed by methods of 

multi-factor analysis. In the absence of drought the sawfly density is low and fluctuates within the 

steady state. Density regulation described by coefficients of m- and v-stability is associated with 

host-parasitoid interactions. Parasitoids developing in eggs and those in eonymphs prevent the change 

of the mean host density level (m-stability), but only parasitoids of eonymphs stabilize host density 

fluctuations (v-stability). Sawfly outbreaks are initiated by droughts which weaken the host plant and 

interrupt eonymph diapause. Both increase and decrease of sawfly density during the outbreak are 

caused by process interactions rather than individual processes. In the postoutbreak period, repeated 

drought cannot initiate a new outbreak because of high eonymph-parasitoid density. In general, the 

outbreak character of sawfly population dynamics is associated with the presence of egg parasitoids that 

suppress but destabilize the host density. The role of each ecological process is determined not only 

by its own properties but by the whole life system including the population and its effective 

environment. The role of processes in population dynamics should be analyzed using simulation 

models that can describe adequately the interaction of these processes in the life system. 

ACKNOWLEDGMENTS 

I would like to thank Dr. N.A Tamarina, Dr. V.N. Maximov, and Dr. N.M. Chernova for their 

discussion of my work. 

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198 
BIOECOLOGY OF THE CONIFER SWIFf MOTH, 

KORSCHELTELLUS GRACILIS, A ROOT FEEDER 

ASSOCIATED WITH SPRUCE-FIR DECLINE 

WILLIAM E. WALLNER 1 

DAVID L. WAGNER2 

BRUCE L. PARKER3 and DONALD R. TOBI3 

1USDA Forest Service 

Northeastern Forest Experiment Station 

51 Mill Pond Road 

Hamden, Cf 06514 U.S.A 

2University of Connecticut 

Department of Ecology and Evolutionary Biology 

Storrs, Cf 06268 U.S.A 

3University of Vermont 

Department of Plant and Soil Science 

Burlington, VT 05401 U.S.A 

INTRODUCTION 

During the past two decades, the decline of red spruce, Picea rubens Sargent, and balsam fir, 

Abies balsamea (L ), at high elevations (900-1200 m) in eastern North America has evoked concern 

about the effects of anthropogenic deposition upon terrestrial ecosystems. In many high-elevation 

forests across New England, as many as 50 percent of the standing red spruce are dead (Hertel et al. 

1987). Wood cores indicate that growth has been severely curtailed since the 1960s (Hornbeck and 

Smith 1985). Although acid rain is most commonly invoked as the principal causal agent of this 

decline, there is yet little hard evidence to support this claim (Johnson and Siccama 1983, Pitelka and 

Raynol 1989). A wide array of anthropogenic pollutants in combination with natural stress factors are 

probably involved. Above-ground portions of declining trees appear relatively pest free, and so do the 

roots except for observations of a few soil-inhabiting arthropods. The most prevalent among those few 

was a subterranean lepidopteran polyphage, Korscheltellus gracilis Grote, found to be extremely 

abundant in these declining forests (Tobi et al. 1989, Wagner et al. 1987). A member of the 

Hepialidae family, K. gracilis is relatively unknown both in habit and distribution. In North America, 

documented knowledge about the biology or feeding habits of Hepialidae is limited to cursory reports 

on Sthenopis argenteomaculatus Harris as a borer in maple, oak, chestnut, and alder (Felt 1906). 

Sthenopis quadriguttatus Grote bores into the roots of aspen, cottonwood, and willow (Furniss and 

Carolin 1977, Gross and Syme 1981). Only one species, Hepialus mustelinus Packard, has been 

reported as a borer in spruce (Felt 1906, Packard 1895). In Australia the Hepialidae are among the 

major pests feeding on pasture grasses (Tindale 1933), and as stem borers of living trees (Tindale 

1953), and tree roots (Tindale 1964). 

BARANCHIKOV, Y.N., MATfSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

199 
Adults of K gracilis occur from June through early August and are active for 20 to 40 minutes 

during evening and dawn twilight. Inactive during the day, the cryptically marked adults rest on tree 

trunks or foliage. Eggs, scattered by females while in flight, hatch in 2 to 4 weeks. The whitish, 

unornamented larvae pass through two winters, attaining lengths of 35 to 45 mm before pupating in 

the upper layer of forest litter. At all locations where we studied this insect, abundance and marked 

scarcity of adults alternated from year to year, thereby suggesting a 2-year cycle. 

Our studies represent an attempt to clarify the relationship of K gracilis to its hosts, explain its 

apparent abundance in high-elevation forests, and increase information about its bioecology. 

EXPERIMENTAL APPROACH 

Densities and distribution of K gracilis were determined in high-elevation forests in Vermont, 

New York, and New Hampshire, and at a sea level site of red spruce in Saulnierville, Nova Scotia. 

Quantitative estimates of larval and pupal densities were based upon examination of a series of 

0.25 m2 soil pits at elevations of 500, 700, 900, 1,100, and 1,300 m on Whiteface Mountain in New 

York and Mt. Moosilauke in New Hampshire. Two plots consisting of five subplots each were used to 

count fall and spring larval densities at each location-exposure. The relative abundance of adults was 

estimated by using two interception traps (1/4-m2 sheets of clear plastic coated with Tanglefoot) placed 

50 em off the ground. On each mountain, plot transects were deployed at the point of maximal 

exposure to cloud base impact and on the lee side. 

We measured feeding preference and seedling damage trials in the laboratory using fieldcollected mid-instar larvae 2 to 3 em in length (Grehen et al. in press). Survival and weight gain on 

the predominant food sources available to this polyphage at high elevations and bordering lower 

elevation sites were evaluated to clarify relative suitability. In addition, three groups of 20, 2-year-old 

red spruce seedlings were inoculated with 0, 1, or 3 mid-instar larvae in the field at elevations of 700, 

900, and 1,100 m. Seedlings were planted with their roots enclosed in saran screening so as to confine 

inoculated larvae within soil around the roots. This not only prevented larval escape, but also 

prevented other K gracilis larvae or organisms from attacking the roots of the seedlings. 

Periodically, larvae were collected from all sites, brought to the laboratory, and reared 

individually on carrots to enable us to rear out natural enemies. 

RESULTS AND DISCUSSION 

Densities of larval and adult K gracilis were consistently highest at 900 and 1,100 m, and lowest 

below and above these elevations (Fig. 1 ). Mixed hardwood predominates below 700 m, whereas the 

proportion of spruce-fir increases from 700 to 1,100 m, and red spruce declines as balsam fir increases 

up to 1,300 m. There are few if any trees above 1,300 m. The abundance of K gracilis corresponds 

roughly with that of red spruce, together with maximal tree decline and cloud-based impact. In the fall 

of 1987, larval densities were extremely high at Whiteface Mountain, New York, and Mt. Moosilauke, 

New Hampshire; estimated densities at 900 m were 5.6 and 14.8 larvae/m2, respectively. At these two 

sites, however, larval densities declined over winter by 51 percent and 72 percent, respectively (Fig. 2). 

The Hepialidae are extremely polyphagous and K gracilis is no exception. Field observations 

verified larval feeding upon woody and nonwoody roots of red spruce and balsam fir. Seedling 

inoculation experiments (Fig. 3) demonstrated that larvae significantly affect root area and root weight 

at all elevations studied. Interestingly, the roots of uninfested seedlings had greater area and higher 

weight as elevation increased. Dieback of seedlings was most pronounced at 700 m with larval 

densities of three larvae/seedling. 

200 
14 

w 12 

~ 10 ~ La.. 8 

0 

~ 

w 6 

m 

:::E 

:::> 4 

z 

z 2 ~ ::!! 0 

-2 

•--•Whiteface Mt. - Lee 

0--0Whiteface Mt. - Exposed 

•-• Mt. Moosilauke - Lee 

0-0 Mt. Moosilouke -•<0 

0 ,-"' 

/ ... o-................ 

.......... ·~ 0 

~v -- ;-- --------------=::.-:::.. 

500 700 900 1100 1300 

ELEVATION (METERS) 

Figure 1. Fall distribution of the conifer swift moth, Korscheltellus 

gracilis, by elevation and location. 

With naturally occurring densities of K gracilis often averaging 101m2, it is very probable that 

larvae significantly reduce both spruce and fir regeneration. 

In laboratory rearings on 10 potential food sources found in the high-elevatiOJ!. forests, K gracilis 

accepted most of those offered (Table 1 ). Only in rotten wood did larvae fail to survive. The other 

food sources with which survival was greater than 50 percent were those commonly found in highelevation forests. Sugar maple commonly occurs in mixed stands below 700 m; whereas white birch 

occurs in forests up to 1,200 m and mountain ash is common up to 900 m, but their proportion is low 

between 700 and 1,200 m. It is interesting to note that red spruce and balsam fir were once common 

at lower elevations, but are now more restricted to the higher elevations. Densities of K gracilis are 

highest at elevations where spruce and fir dominate, and its survival is best on these hosts. Its poor 

performance on deciduous species may influence K gracilis distribution and indicate that it is a weak 

polyphage. 

It is generally accepted that larval weight gain over time (expressed as weight change from 

initial) is a reasonable indicator of host suitability. In our studies, carrot yielded not only highest 

survival but also weight gain, probably because it contains high protein and low toxic chemical levels. 

Another tuberous species, Dryopteris fern, a common component of high-elevation spruce/fir stands, 

showed relatively low percentages of survival and weight gain. Larvae commonly tunnel into the roots 

of fern in the field, but our data suggest that it is only marginally suitable. Weight gain on spruce and 

fir was equivalent to relative growth rates of 0.03 mg/mg/day. These growth rates are low for 

Iepidoptera, but not unusual since tree roots are low in nitrogen (Slansky and Scriber 1985). 

201 
w 

~ 0:: 

:3 

lL. 

0 

0:: 

w 

m 

~ 

:::> 

z 

z 

~ ~ 

14 

12 

10 

8 

6 

4 

2 

0 

-2 

•--•Whiteface Mt. - Lee 

0--0Whiteface Mt. - Exposed 

•-• Mt. Moosilauke - Lee 

0-0 Mt. Moosilauke - Exposed 

500 700 900 1100 

ELEVATION {METERS) 

1300 

Figure 2. Spring distribution of the conifer swift moth, Korscheltellus 

gracilis, by elevation and location. 

Table 1. Average survival and weight gain for the conifer swift moth reared 

on ten hosts 

Host 

Carrot 

Moss 

Fir 

Hairy moss 

Red spruce 

Ash 

Birch 

Fern 

Sugar maple 

Rotten wood 

Percent 

survival 

85.00 

70.00 

61.11 

60.00 

55.56 

44.44 

33.33 

33.33 

17.65 

0.00 

Percent 

weight gain 

817.6 

302.4 

79.6 

277.0 

93.2 

1.4 

105.1 

32.8 

60.8 

202 
100 

Larval Larval Larval 

number number number 

03 03 83 

11 11 11 

oo DO oo e s u 

E i .2» 

J ta50 ! 

8 -

"' a: 8 

1 a: 

700 900 1100 

Altitude (m) 

Figure 3. Response of red spruce seedlings to different densities of 

Korscheltellus gracilis larvae at different altitudes on Mt. Mansfield, VT. 

The impact of K gracilis feeding on roots .of mature trees is less clear. We have observed larval 

root damage on numerous spruces and firs. In one case, a 50-year-old balsam fir contained more than 

30 feeding scars. The larvae feed through the bark, but do not penetrate deeply into the xylem, 

creating elongate lesions along the axes of second to fourth order roots, fascicles of orange-brown frass 

and wood chips accumulating on either side of the wound. Such feeding sites provide entry courts for 

pathogens or nematodes. In fact, a wood-staining fungus has been found in association with K gracilis 

feeding wounds in Vermont (Dale Bergdahl, pers. comm. ). 

The spruce-fir decline at high elevations in eastern North America is a complex process 

involving several factors. The fact that K gracilis larvae occur at high densities in declining forests 

suggests that they may reduce tree regeneration and produce large numbers of feeding wounds on 

mature trees and thus may be one of those factors. Trees weakened by air pollution may subsequently 

be attacked by K gracilis, or pollution-induced changes in the chemistry of the soil environment may 

permit unusual increases in the population of the insect, which then damages healthy trees. 

LITERATURE CITED 

FELT, E.P. 1906. Insects affecting park and woodland trees. N.Y. State Mus. Mem. 8(2): 1-721. 

FURNISS, R.J. and CAROLIN, V.M. 1977. Western forest insects. U.S. Dep. Agric. For. Serv. Misc. 

Publ. 1339. 

GREHEN, J.R., PARKER, B.L, WAGNER, D.L, ROSOVSKY, J., and ALEONG, J. In press. 

Seedling root damage by conifer swift moth larvae: a potential factor in high elevation red 

spruce decline. 

203 
GROSS, H.L. and Syme, P.O. 1981. Damage to aspen regeneration in northern Ontario by the ghost 

moth, Sthenopis quadriguttatus. Can. For. Serv. Res. Notes 1(4): 30-31. 

HERTEL, G.D., ZARNOCH, S.J., ARRE, T., EAGAR, C., MOHNEN, V.A, and MEDLARZ, S. 

1987. Status of the spruce-fir cooperative research program. 80th Annu. Mtg. APCA (Air 

Pollution Control Association); 21-26 June, New York, NY. 87-34.2: 1-19. 

HORNBECK, J.W. and SMITI-1, R.B. 1985. Documentation of red spruce decline. Can. J. For. Res. 

15: 1199-1201. 

JOHNSON, AH. and SICCAMA, T.G. 1983. Acid deposition and forest decline. Environ. Sci. Tech. 

17: 294-305. 

PACKARD, AS. 1895. On the larvae of the Hepialidae. J. N.Y. Entomol. Soc. 3: 69-73. 

PITELKA, L.F. and RAYNOL, D.J. 1989. Forest decline and acidic deposition. Ecology 70: 2-10. 

SLANSKY F. and SCRffiER, J.M. 1985. Food consumption and utilization, pp. 87-163. In Kercut, 

G.A and Gilbert, L.I., eds. Comprehensive Insect Physiology and Pharmacology, Vol. 4. 

Pergamon Press, New York. 

TINDALE, N.B. 1933. Revision of the Australian ghost moths (Lepidoptera, Homoneura, Family 

Hepialidae). II. Rec. S. Aust. Mus. 5: 14-43. 

TINDALE, N.B. 1953. On a new species of Oenetus (Lepidoptera, Family Hepialidae) damaging 

Eucalyptus saplings in Tasmania. Trans. Roy. Soc. Aust. 76: 77-79. 

TINDALE, N.B. 1964. Revision of the ghost moths (Lepidoptera, Homoneura, Hepialidae). VIII. 

Rec. S. Aust. Mus. 14: 663-668. 

TOBI, D.R., WALLNER, W.E., and PARKER, B.L. 1989. The conifer swift moth, Hepailus gracilis, and 

spruce-fir decline, p. 351-354. In Proc. U.S.-F.R.G. Symposium: Effects of atmospheric pollutants 

on the spruce-fir forests of the eastern United States and Federal Republic of Germany. 

U.S. Dep. Agric. For. Serv. Northeast. For. Exp. Stn. Gen. Tech. Rep. 

WAGNER, D.L., PARKER, B.L., and WALLNER, W.E. 1987. Red spruce decline in New England: 

are swift moths the culprits? Vermont Sci. 11: 1-4. 

204 
THE RECONSTRUCfiON OF L YMANTRIA DISPAR 

OUTBREAKS BY DENDROCHRONOLOGICAL METHODS 

IN THE SOUTH URALS 

SERGEIKUCHEROV 

Institute of Plant and Animal Ecology 

Ural Branch of the U.S.S.R. Academy of Sciences 

Sverdlovsk 620008 U.S.S.R. 

INTRODUCTION 

Interest in investigating the influence of extreme ecological factors on the radial growth of oak 

(Quercus robur L.) is bound up with oak dieback in the South Urals during the last decade. Factors 

contributing to this problem in the study area are hard winter frosts, late spring frosts, and Lymantria 

dispar L outbreaks. To distinguish the influence of these factors on radial growth, I used a 

methodological approach involving the analysis of radial increment, anatomical structure of xylem, 

histograms of ring indexes, and comparative analysis of radial growth in different plots (Kucherov 1987, 

1988). By means of dendrochronological analysis, I was able to determine which specific features of 

radial increment were influenced by different factors (Kucherov 1988). 

RADIAL INCREMENT RESPONSE TO DEFOLIATION 

I found that maximal reduction of radial increment occurred following pest outbreaks during 

which the level of defoliation reached more than 70 percent. When defoliation did not exceed 

50 percent, reduction of radial growth was not observed. The character of radial increment, further, 

depended on the degree of leaf regeneration after defoliation. When secondary leaves did not form, 

maximal decrease in radial increment took place in the year following defoliation (an after-effect). On 

the other hand, when secondary leaves did form, the after-effect was negligible or absent. The period 

of radial growth reduction, depending on the level of canopy recovery, was 1 to 2 years. Long periods 

of mean radial increment reduction were observed only in suppressed trees. Some of these trees 

( 4 percent after the outbreak in 1985) were drying up. The late spring frosts, which also damaged the 

leaves, caused less radial increment reduction than gypsy moth defoliation. 

The radial increment patterns I identified allowed for reconstruction of growth limiting 

determinant events since 1848. It was established that 13 outbreaks have taken place between 1848 

and 1989. Intervals between the subsequent outbreaks were as follows: 11, 10, 12, 13, 12, 14, 11, 12, 

6, 12, 11, and 9 years (the mean being 11 years). I discovered that in the last 50 years a significant 

increase in outbreak intensity had occurred relative to the preceding 90 years. 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

205 
LITERATURE CITED 

KUCHEROV, S.E. 1987. Lymantria dispar outbreaks' effect on radial growth of Quercus robur L in the 

South Urals, p. 285-288. In Dendrochronological methods in forest science and ecological 

forecasting. Thesis of the International Workshop. Irkutsk. 

KUCHEROV, S.E. 1988. The influence of pest outbreaks and climatic factors on radial growth of 

trees. Avtoreferat dissertatsii. Sverdlovsk. 24 p. (In Russian.) 

206 
IMPACT OF A SPRING DEFOLIATOR 

ON COMMON OAK 

VICfOR V. RUBTSOV and IRINA A UTKINA 

Forest Science Laboratory 

Moscow Branch of the U.S.S.R. Academy of Sciences 

Uspenskoe, 143030 U.S.S.R. 

INTRODUCTION 

We have investigated the population dynamics of some common phyllophagous insects in oak 

stands of the forest-steppe zone and their impact on common oak (Quercus robur L ). Considerable 

attention has also been paid to mathematical modeling of the studied processes. All field data 

represent samples taken from the Tellerman oak grove in the Voronezh region, where repeated 

observations have been made from 1969 up to the present. Our particular concern is the green oak 

leaf roller (Tortrix viridana L ), which propagates in 70 to 100-year-old oak stands in the floodplain of 

the region. 

Fig. 1 shows characteristics of the weather conditions from 1969 to 1988 as well as results of 

field observations and mathematical modeling of the oak leaf roller's population density and the 

defoliation of oak crowns. More detailed description of methods and discussion of results are given in 

Rubtsov (1983) and Rubtsov and Rubtsova (1984). Last year's data showed that in all oak forests in 

the region significant number of eggs died during the summer to autumn period. That alters our 

conception of the egg stage of the oak leaf roller as its most favorable stage, subject only to high 

mortality during severe and prolonged frosts. 

DEFOLLATIONI~ACTS 

Our investigations show a close relation between degree of defoliation of a stand and the ratio 

of late wood/early wood. For example, after 20 percent defoliation, this ratio is about 3:5, whereas 

after 80 percent defoliation, it is only about 1:4. 

We have studied the defoliation of oaks damaged by spring phyllophagous insects since 1984. 

Larval feeding on oak foliage varies with weather conditions but usually lasts 18 to 24 days. Foliage is 

destroyed both in buds and on growing shoots. Depending on different combinations of environmental 

conditions, trees features, and insect populations, the defoliations have different effects, causing 

substantial variability in refoliation processes. 

We divided all shoots that regrew after defoliation into replacement shoots (from reserve and 

dormant buds) and secondary shoots (from new buds). In most of the cases, the crowns of defoliated 

oaks have both kinds of shoots. According to our data, the greater the degree of defoliation and the 

faster it is reached, the earlier a tree begins to refoliate and the greater the proportion of replacement 

shoots among the regrowth. As larvae began feeding in the upper parts of the crowns, defoliation of 

the upper two-thirds of the crowns was 80 to 100 percent and that of the lowest one-third only 30 to 

BARANCHIKOV, Y.N., MATrSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

207 
2~0 --1 

---2 

t&D ···········3 

0 ~ 110 ... :z 

0 60 ..__ 

c:c 

> 0. 

l&J 

-==- -60 

X ~0 -i B 

u 

z ---2. 

< 

~ 

c:O 

~ 2.0 

~ 

IJ) 

~ 

U1 

uJ 0 

~ 100 c 

z - --4 

c ---2. 

1- 60 

c 

-l 

0 

La. 20 ..... 

~ 0 

1970 1g75 1980 i985 YEAR 

Figure 1. Weather conditions, oak leaf roller population density, and 

defoliation of oaks in the Tellerman oak forest from 1964 to 1988. 

A) hydro-thermal coefficient (HTC) deviations from the average values of many 

years: 1) HTC of May, 2) HTC of growing season (May to September), 3) annual 

HTC; B) oak leaf roller population density: 1) field data, 2) calculated 

data; C) oak stands defoliation: 1) field data, 2) calculated data. 

80 percent. In the latter case, secondary shoots were predominant. The greater the degree of foliage 

survival, moreover, the larger the share of secondary shoots among the regrowth. Since secondary 

shoots start growing later than replacement ones and have the lower growth rate, we can surmise that 

trees with a predominance of secondary shoots sustain a longer period of reduced foliage area. 

Our 4-year observations show that trees with different degrees of defoliation have different 

numbers of reserve and dormant buds per 1 m of twigs at the end of summer. These findings are 

discussed at greater length by Utkina and Rubtsov (1989). Fig. 2 shows the average decrease in 

nongrowing buds for trees of slight and severe defoliation respectively. One can see that with slight 

defoliation (about 30 percent), the density of such buds is quite stable, whereas with severe defoliation 

208 
A G 

ItO 

-o-i 

---2 

Cl) 

\.!1 

0 

tLa. 

~ 

- ~0 

0 

~ 

s: 

._... ~0 

.........___ 

V) 20 ~ 

~ 

cO 

0 

MAY JUN JUL. AU& MAY JUN JUL. AU'i MAY JUN JUL. AUGFigure 2. Numbers of nongrowing (reserved and dormant) buds in oak trees with 

30 to 50 percent defoliation (1) and 75 to 100 percent defoliation (2). 

A), B), C), and D) 85-year-old stand from 1986 to 1989; E) and F) 105-year-old 

stand from 1987 to 1988. 

(75 to 100 percent) the density of nongrowing buds declines from year to year. This is related to the 

fact that reserve buds open after defoliation, while some of them would be able to fill up the pool of 

dormant buds. Moreover, some share of the nongrowing reserve buds dry out in summer and fall. 

Fig. 3 shows the share of dead reserve buds to be largely independent of degree of defoliation. 

Comparison of foliage weight and area per 1 m of twigs in oak trees sustaining different degrees of 

defoliation suggests that, in general, refoliation is completed in defoliated crowns by the end of growing 

season. 

One of the chief difficulties of mathematical modeling, especially of simulation modeling, is the 

weak data sets. In addition to such real deficiencies, moreover, there are methodological problems: 

inadequate structure and volume of data because of discrepancies between the final aim of the 

investigation, model structure and organization, and the system of field data sampling. 

ACKNOWLEDGMENTS 

The authors wish to thank Svetlana S. Puzyr for her expert editorial and clerical assistance as 

well as Dr. Y.N. Baranchikov for his editorial review. 

209 
~0 c 

rr- ,- r10 1-

0 MAY JUN JUL AUG 

~ ~ol D ............... 

~ ~ ~ 

MAY JUN JUL AUG MAY JON JUL. 

r- • 1 1- r- E 0 2 

~ 3 r1- r- ,--

.- rI'-

! 

~ I -- ~ ~L- MAY JUN JUL AUG MAY JUN JUL AUG 

Figure 3. Numbers of reserved buds: in oak trees with 30 to 50 percent 

defoliation (left columns) and 75 to 100 percent (right columns). 1) alive, 

nongrowing; 2) dead; 3) buds grown after defoliation. A), B), and 

C) 85-year-old stand from 1987 to 1989; D) and E) 105-year-old stand in 

1987-1988. 

LITERATURE CITED 

RUBTSOV, V.V. 1983. Mathematical model for development of leaf-eating insects (with special 

reference to oak leaf roller). Ekol. modelirovanie 18: 269-289. (In Russian.) 

RUBTSOV, V.V. and RUBTSOV A, N.N. 1984. Analysis of leaf-eating insects-oak relations. Analiz 

vzaimootnoschenii listogryzuschikh nasekomykh i duba. Nauka, Moscow. 1833 p. (In Russian.) 

UTKINA, I.A and RUBTSOV, V.V. 1989. Bud bursting and shoot regeneration in oak tree after 

defoliation accomplished by insects. Lesovedenie 3: 46-54. (In Russian.) 

210 
TOLERANCE TO INSECT DEFOLIATION: 

BIOCENOTIC ASPECTS 

ANDREY A PLESHANOV, VICfOR I. VORONIN, 

ELENA S. KHLIMANKOV A, and VALENTINA I. EPOV A 

Siberian Institute of Plant Physiology and Biochemistry 

Siberian Branch of the U.S.S.R. Academy of Sciences 

Irkutsk 664033 U.S.S.R. 

INTRODUCTION 

Woody plant resistance to insect damage is of great importance in forest protection, and tree 

tolerance is an important element of this resistance. 

The compensating mechanisms responsible for tolerance are nonspecific as a rule and develop 

after damage has been caused by phytophagous animals or other unfavorable effects. Beyond that, 

plant tolerance depends on duration, repetition, and phenological periods of the damage effects, and on 

environmental conditions. We have studied of radial increment patterns in trees as a measure of their 

physiological state. 

This approach may be tested in areas infested by various dendrophagous species and is especially 

useful if the outbreak areas are vast, similar dynamics prevail in different forest site conditions, and the 

damage inflicted generally does not cause tree mortality. In these respects, the areas infested by 

Zeiraphera griseana Hbn., Dasychira abietis Schiff., Pygaera anastomosis L, and Leucoma salicis L 

represent potentially significant conditions for estimation of the defoliation tolerance of larch, pine, and 

aspen trees, respectively, in Eastern Siberia. 

TREE GROWTH RESPONSES TO DEFOLIATION 

Fig. 1 shows the dynamics of radial increment of Larix sibirica in two biotopes that contrast in 

heat and water supply. The first curve shows the decrease in the increment caused by Zeiraphera 

griseana Hbn. defoliation in central larch taiga forests. Tree damage in 1953 and 1971 resulted in 

increment decline for the next 5 to 7 years. The second curve shows that Zeiraphera griseana 

outbreaks were more frequent in larch forests in the forest-steppe zone: in 1930, 1943, 1949, 1953, 

1959, 1963, 1967, 1971, 1975, 1981, and 1987 (Fig. 1, curve 2). However, the increment decline 

following each defoliation was recorded over only 1 to 2 years. The same stand was also damaged by 

Erannis jacobsoni Djak. in 1964 and 1971. The consequences of that insect defoliation were registered 

over 5 years. This comparative geobotanical approach appears to be useful for mapping differential 

forest tolerance to phyllophagous insects. 

The practical importance of such maps is evident given the importance of wood increment 

decrease as an indicator of the economic significance of phytophage outbreaks and the efficiency of the 

BARANCHIKOV, Y.N., MA1TSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

211 
120 

100 

l£.1 

..:I 80 

< 

u 

en 

~ 

0 60 

20 

A 

I '' I 

I l 

I I 

I I 

I ' A 1 ,,, I \I\ ' 1 ' ' : ~ \ ,,, ,, \ 

1 1\ ,, ' 

I ~ lh I l lJ 

'•' \1 • '1 \\I lJ 

~ ' 

---1 

----2 

• J 

X 4 

YEARS 

Figure 1. Fragment of dendrograms of Larix sibirica from different biotopes; 

1. larch forests in the forest-steppe zone; 2. larch forests in the central 

taiga zone among herbs; 3. years of defoliation by larch bud moth; 4. years of 

defoliation by Erannis jacobsoni Djak. 

proposed forest protection measures. In addition, tolerance is directly related to the possibility of 

further tree damage by insects. The depression of physiological processes caused by defoliation results 

in temporary (passive) immunization of trees to a number of pests. Knowledge about the length of 

the immunization period--readily acquired through study of radial increment in damaged trees--would 

also contribute to better planning of forest protection measures. 

Moreover, identification of the areas having high outbreak frequency is necessary for 

organization of forest pathological monitoring. Dendrochronological data may be used also for 

retrospective analysis of insect outbreaks. 

212 
INSECT-PLANT INTERACTIONS IN 

ANTHROPOGENICALLY TRANSFORMED ECOSYSTEMS 

EVGENY V. KOLTUNOV, VICfOR I. PONOMAREV, 

and SERGEY I. FEDORENKO 

Institute of Forest 

Ural Branch of the U.S.S.R. Academy of Sciences 

Sverdlovsk U.S.S.R. 

INTRODUCTION 

Structural and functional changes in forests due to anthropogenic factors have a considerable 

impact on the interaction of phytophagous insects with the phytocenosis. Many features of these 

processes have yet to be investigated in the deciduous forest conditions of the forest-steppe zone. 

We investigated birch forests disturbed by anthropogenic factors in the middle and southern 

Urals. Anthropogenic transformation stages were determined using geobotanical analyses of grass 

(Polyakova 1983), physiological and chemical analyses of soil, and analyses of forest stand structures 

and the dynamics of radial increment growth. The principal subject of study was Lymantria dispar 

populations over the course of a population cycle. 

INSECf POPULATION LEVELS 

Analysis of the forest plots inside and outside outbreak centers showed that both suffered 

equally from pervasive anthropogenic impacts. The mean level of degradation was extremely high. No 

undisturbed forest plots were found. 

The level of anthropogenic impact determines to a large extent the spatial distribution of 

Lymantria dispar outbreak centers. Thus egg density and caterpillar distribution correlate closely with 

the different stages of anthropogenic transformation: in the most disturbed forests (the fifth stage) a 

high population density and complete defoliation were caused by caterpillars. Pests attacked the least 

disturbed forest plots at the first stage as well, but population density and degree of defoliation were 

minimal there. We found a consistent difference in insect populations (mean weight of gypsy moth 

pupae, and adults, the sex ratio of moth) inhabiting the birch forests, at the first to second and the 

fourth to fifth stages of degradation. As degradation increased, we observed a concomitant increase in 

insect development rate. 

The extent of anthropogenic transformation level also effected the activity of parasites and 

pathogens in gypsy moth populations. The natural mortality of late-instar larvae due to nuclear 

polyhedrosis was 42 percent higher in forest plots at the fourth stage than in the third stage; tachinid 

and ichneumonid parasitism was four times higher. In low-density birch stands significantly disturbed 

by anthropogenic factors, gypsy moth larvae tend to occur mainly on trunks and branches and to 

disperse by wind in the second instar, thus reducing the population density. 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

213 
FOREST RESPONSES TO DEFOLIATION 

The forest reaction to defoliation is largely determined by the mean level of its anthropogenic 

transformation: at the same degree of defoliation the forest stand reaction correlates with the stages of 

anthropogenic dynamics. In weakly disturbed forest stands (at the first and second stages), Lymantria 

dispar does not cause complete defoliation and no structural transformation is evident except for a 

10 percent growth loss, which may be caused by the dispersal of larvae to more degraded forest plots. 

At the third and later stages of the anthropogenic dynamic, forest reaction includes two substantially 

different developments: rapid death (within a year of defoliation) and slow death (over several 

subsequent years). Duration of the second response increases significantly in the most degraded forest 

plots. At third to fifth stages, total forest stand mortality in the gypsy moth outbreak centers in the 

Middle and Southern Urals was 10 to 20 percent and 0 to 10 percent at third stage, 20 to 40 percent 

and 10 to 20 percent at the fourth stage, and 40 to 80 percent and 20 to 50 percent respectively, at 

the fifth stage. In some forest plots, total mortality reached 100 percent of the forest stand, and the 

area of these forests increased substantially in the 2 or 3 years after the outbreak. Intensive bogging 

and 40 to 60 percent mortality of forest stand were observed after defoliation. Thus the most 

significant result of severe degradation is protraction of the defoliation after-effect and, as a further 

result, continued structural transformation of biogeocenoses. Among other reasons, this may be 

explained by a drastic drop in forest resistance, causing the increase in the biogeocenosis relaxation 

time. 

Inside the outbreak centers there were plots which were infested with a tree bacterial disease 

caused by Erwinia multivorum. Analysis of the concurrence of these two processes shows an additive 

effect taking place. The most important after-effect of the outbreak is the consistent level of tree 

diseases in the forest stand just following the outbreak. Another important outbreak after-effect is the 

intensive attack by xylophagous insects on trees weakened by defoliation, the result of which is 

accelerated tree mortality. 

In sum, the level of anthropogenic transformation of birch forests in the forest-steppe zone 

determines to a large extent the population dynamics of gypsy moth populations and the kind of 

phytocenosis reaction. That is why the monitoring of disturbed deciduous forest ecosystems stratified 

into different anthropogenic transformation stages may be a strategically important means of improving 

forest protection. It may also be used as a method of predicting forest resistance and the dynamics of 

anthropogenic ecosystems. 

214 
DOES THE PLANT DEFEND ITSELF 

AGAINST LEAF-FEEDING INSECfS? 

PAUL M. RAPES 

Laboratory of Forestry, Uspenskoje Village 

Odintzovo Region, Moscow Territory 143030 U.S.S.R. 

Trees do not actively respond to herbivore grazing, they react to the deterioration in the balance 

of their roots and crowns functions, which comes when transpiration powers fall off. Such inherent 

reactions of plants originated as abilities to restore photosynthesis. 

THE LARCH BUDMOTH SYSTEM 

For example, every 9 years the larch budmoth, Zeiraphera diniana On., depletes the subalpine, 

larch-cembran pine forests (Baltensweiler and Fischlin 1988). The heaviest defoliations occur at 

altitudes of 1600-2100 m, last 2.93 + 0.21 years, and recur at intervals of 8.47 + 0.27 years. At lower 

altitudes defoliation occurs half as often and rather irregularly. Close scrutiny has shown that larch 

trees defoliated more than 50 percent refoliate in a manner similar to trees that have suffered from 

frost. In the spring following defoliation, needles are shorter than normal with increased raw fiber and 

decreased protein content. From 2 to 7 years after the outbreak, the needles recover their average 

quality, and the bud moth populations begin to grow along with the parasites which follow them. In 

the growth phase of the population cycle, the bud moth females lay 116 + 19.1 eggs. Total generation 

mortality is approximately 90 percent and that gives rise to a 10-fold increase from one generation to 

the next. In the decline phase, the females lay 12.5 + 19.1 eggs, larval parasitism increases 10-fold and 

the total mortality rises to 99.98 percent. Dendrochronological data observed in fossil larch dating 

from Roman times and in the beams of 15th century farm houses show that larch is adapted to 

defoliation and therefore the bud moth here is not a pest. The causes of bud moth density oscillations 

depend on weather, feeding, competition for food, predators, parasites, and pathogens. 

THE GREEN OAK LEAFROLLER SYSTEM 

The analysis of Tortrix viridana outbreaks in oak forests (Rafes 1989) is another example of this 

phenomenon. The devouring of foliage causes a hyperfunction of chloroplasts which restores the 

assimilation capacity to a small degree and only at the beginning of a serious grazing cycle. During 

hyperfunction and further formation of secondary leaves, the tree produces increased quantities of 

phenols and other antibiotics which accumulate in the leaves (Fagerstrom et al. 1987, Haukioja et al. 

1985). The depletion of leaves diminishes the transpiration power of a crown and the water content of 

trees is reduced. During the period of crown depletion a great deal of the gnawed leaves, larval 

excrement, and entomophages fall to the floor; all of them stimulate the extraordinary activity of 

saprotrophs. A chemical analysis of soil at this time demonstrates an elevated content of nitrogen, 

phosphorous, and potassium. After the tortrix larvae pupate, the secondary foliage grows, but amounts 

to no more than 75 percent of the primary foliage. That is why the autumn leaf fall is only somewhat 

below the ordinary level. As a result of imperfect compensation, the growth in tree stem diameter 

BARANCHIKOV, Y.N., MATfSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

215 
drops off significantly. Throughout an outbreak, the enriching of soil with NPK favors to some degree 

the stand condition. But at the same time the accumulation of phenols and other antibiotics in foliage 

has adverse effects. They poison the tortrix larvae, its parasites, the soil, its inhabitants, and affect the 

roots of plants. Investigations in England (Carlisle et al. 1966) have demonstrated that an outbreak of 

T. viridana can bring about the serious change in the soil. 

TAKING THE SYSTEM PERSPECTIVE 

An insect outbreak is a symptom of forest ecosystem dysfunction. The quantitative relations of 

pests, their parasites, predators, and saprotrophs are disturbed, and their behavior becomes uncommon. 

Ecosystem function is suppressed as a whole and incapable of autoregulation. If it is sufficiently 

resilient it can be restored, but this is the matter of time. If it is not resilient, this ecosystem shall be 

changed. 

At the introduction to the workshop "State and Change of Forest Ecosystems," Andersson (1984) 

considered trends of the problem: most attention has been devoted to the ecological importance of 

photosynthesis and the flow of organic matter in the food chains of biophages. But, nutrient formation 

and soil processes are understood imperfectly. In the monitoring of forest ecosystems, especially for 

the prognosis of pest outbreaks, chemical analysis of the dominant plant foliage and of the soils should 

be done for the physiological studies of phytophages and their host plants. 

Ecosystem is the space-time unity in which all of motions are relative; i.e. interdependent. 

Mathematicians modeling ecosystems are forced to make a simplified schematic pattern of the 

interactions, but ecologist are obliged to reveal and to explain the causes of all phenomena occurring 

therein. 

LITERATURE CITED 

ANDERSSON, F. 1984. Forest ecosystem research--past and present trends. State and changes of forest 

ecosystems--indicators in current research. Swed. Univ. Agric. Sci., Uppsala: 11-18. 

BALTENSWEILER, W. and FISCHLIN, A 1988. The larch bud moth in the Alps, p. 332-351. In 

Dynamics of Forest Insect Populations. Plenum, N.Y.-London. 

CARLISLE, A, BROWN, AH.F., and WHITE, E.J. 1966. Litter fall, leaf production and the effects of 

defoliation by Tortrix viridana in a sessile oak (Quercus petraea) woodland. J. Ecol. 54: 65-85. 

FAGERSTROM T., LARSSON S., and TENOW, 0. 1987. On optimal defence in plants. Function 

Ecology: 73-81. 

HAUKIOJA, E., NIEMELA, P., and SIREN, S. 1985. Foliage phenols and nitrogen in relation of 

growth, insect damage, and ability to recover after defoliation, in the mountain birch Betula 

pubescens ssp. tortuosa. Oecologia: 65: 214-222. 

RAPES, P.M. 1989. Folivores outbreaks as a forest biocenosis' disease. p. 4-94. In Bul. MOIP. 

Otd. Bioi. (In Russian.) 

216 
THE ROLE OF PHENOTYPE STRUCfURE 

IN THE POPULATION DYNAMICS OF GYPSY 

MOTH IN THE LOWER DNIEPER REGION 

NIKOLAJ M. DEREVYANKO 

1.1. Shmalgauzen Institute of Zoology 

Ukrainian Branch of the U.S.S.R. Academy of Sciences 

Lenin Street, 15, Kiev, U.S.S.R. 

INTRODUCTION 

One of the characteristic features of the gypsy moth population in the Lower Dnieper area is its 

variable larval coloring. Phenotype frequency has been recorded over the years in separate 

micropopulations at different density levels. The data show the population to consist mainly of gray 

larvae in all life stages, and their abundance varying from 85 to 99.6 percent. Larvae with a black 

stripe along the back (black type) range from 0.4 to 15 percent of the population. Depending on the 

phase of population gradation, the phenotype concentrations in a population can vary. At high and 

low density levels, black stripe larvae are very rare and make up only 0.4 to 1 percent of the 

population, while at the onset of population growth, their relative quantity rises up to 15 percent. 

Thus at the commencement of population growth, when individuals are typically the most viable 

and fecund, relatively large growth is recorded for the black phenotypes. Such a dynamic ratio of 

phenotypes in a population supports Dobrzhansky's (1970) assertion that genotype value is inversely 

proportional to its abundance in a population. 

Hence the question arises of adaptive selective value of black stripe genotype. The data of 

Kolybin and Zelinskaya (1969) and Kolybin (1976) as well as our own show that these black types 

from the areas of different population density differ according to a number of ecological and 

physiological indices. In particular, their higher fecundity, egg weight, and survival rate promotes fast 

population growth. 

GENETIC BASES OF LARVAL COLORING 

We tested the genetic bases of these differences between morphs by crossing different phenotype 

specimens in several generations to obtain data on inheritance patterns of larvae coloration and other 

biological characteristics of broods. The results show that in crossings of gray females and black males, 

or black females and gray males, yield two types of larvae--gray and black striped specimens in a 1:1 

ratio. On the other hand, in crossings of black females and black males also yield two types of larvae 

--gray and black striped, but in a 1:3 ratio. Crossings of gray females and gray males does not yield 

only gray larvae. The test showed larvae coloring to be simply inherited: gray phenotype larvae being 

recessive homozygotes and the black phenotype being determined by the dominant "black" gene. 

Analysis of the phenotype ratios in a population and its changes depending on level of 

population density suggests that in the gypsy moth population we investigated, balanced polymorphism 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

217 
occurs. Essentially, it functions to maintain the most favorable ratio of homo- and heterozygotes in 

the given habitats. It is an adaptive reaction of a population to its environmental conditions evidenced 

in phenotype structure. I should note that a balanced phenotype ratio, inclined toward a predominance 

of gray larvae (homozygotes by coloring), is maintained due to the higher viability of homozygotes in 

certain sets of ecological conditions. Deviations in phenotype ratio occur under conditions deviating 

from the optimal ones. 

ATIRIBUTES OF PROGENY FROM DIFFERENT CROSSES 

Analysis of biological attributes of a phenotype crossing over a number of generations showed 

that in crossings of two gray types, fecundity of the next generation decreases for each, and the average 

weight of an egg increases in a second generation and decreases in the next ones. When we compared 

egg clusters obtained in crossing of gray female homozygotes with black male heterozygotes, the 

fecundity of the progeny turned out to be about two times higher than that of a pairing of 

heterozygotes (P = 0.01), but close to the fecundity index of a pairing of two homozygotes (P < 0.5 ). 

The fecundity index varies depending on the combination of parental pairs by phenotype feature, while 

average egg weight index has a different mode of variability. In all variant crossings of heterozygote 

females average egg weight in the progeny was more than two times higher than that of the 

homozygotes' progeny (P > 0.001 ). 

Of considerable significance is the fact that even in crossings of brothers and sisters, the 

fecundity indices and egg weight values correlate with phenotypes of the parents in the crossing. 

Comparison of the fecundity indices in all progeny of phenotype crossings--a maximum of 544 

eggs and a minimum of 115 eggs--showed that the substantial variability of this index depended on 

parental phenotypes. The coefficient of variation in fecundity is very high, amounting to 61.4 percent. 

On the other hand, that of the average egg weight is only 13.29 percent. 

Data on progeny variability from different parental crossing are of special interest. Beginning 

with the third generation the specimens of gray coloring turned out to be the most viable. The 

viability of gray and black specimens in the laboratory experiment was compared with the phenotypes 

ratio at different stages of population dynamics in nature. These data showed population heterogeneity 

to increase owing to a greater probability of sexual encounter between different phenotypes. This may 

lead to increase in both viability and fecundity and, consequently, to greater population density. 

In subsequent generations, when population density increases, the probability of sexual encounter 

between hetero- or homozygotes decreases owing to the greater frequency of homozygotes. However, 

the achieved potential for viability increases owing to phenotype hybridization and promotes both 

population growth and outbreak. Population abundance decreases with the overcoming of high 

heterogeneity. 

LITERATURE CITED 

DOBRZHANSKY, T. 1970. Genetics of the evolutionary process. R. V.: Columbia Univ. Press. 505 p. 

KOL YBIN, V.A 1976. Role of population structure and intrapopulational heterosis in the population 

dynamic of Porthetria dispar. Zool. Zh. 55(6): 844-855. (In Russian.) 

KOL YBIN, V.A and ZELINSKA Y A, L.M. 1969. Ecological and physiological peculiarities of 

Porthetria dispar L population in the Lower Dniepr area. Communication 1. Structure of 

population. V estn. Zoo I. 3: 37-42. (In Russian.) 

218 
NOVEL ASPECfS OF HOST TREE 

RESISTANCE TO LEAFMINERS 

STANLEY H. FAETH 

Department of Zoology 

Arizona State University 

Tempe, AZ 85287 U.S.A 

INTRODUCTION 

At least 10,000 species of Ieafminers in four orders of insects (Lepidoptera, Diptera, Coleoptera, 

and Hymenoptera) are found worldwide. The common feature of all Ieafminers is that larvae feed 

within leaves for at least some larval stages. Larvae of facultative mining species feed internally but 

also externally as free-feeders, usually in later larval instars. Larvae of obligate mining species feed 

exclusively, and may also pupate, within leaves (Hering 1951, Powell 1980). Despite wide interspecific 

variation in life histories, leafminers are generally more closely associated with their feeding substrates 

than are free-feeding insects (Mattson et al. 1988). This "intimacy" (sensu Mattson et al. 1988) is the 

primary factor in directing their evolution and influencing population dynamics. 

For leafminers, as distinct from most free-feeding insects, selection of feeding substrates is 

determined solely by female oviposition choice, at least for obligate leafminers. Eggs may be cemented 

to the surface or embedded in the leaf, so adult females determine feeding sites not only among plants 

but also within leaves. For facultative leafminers, female oviposition choice determines larval feeding 

sites for at least some larval instars, and female choice generally plays a much larger role in larval 

feeding sites than it does for most external feeding insects. Confinement to a single leaf means that 

larvae cannot behaviorally escape deteriorating abiotic or biotic conditions associated with their 

substrates as vagile insect larvae can, though a few species can mine more than one leaf by exiting the 

mine or mining through the petiole to adjacent leaves. The individual leaf is the arena where the fates 

of larvae are decided. 

Because of this tight link between oviposition and larval feeding sites and survival, one expects 

strong selection on female oviposition choice. Since many free-feeding larvae are mobile, however, 

oviposition choice may be less critical. Furthermore, since most adult lepidopteran leafminers do not 

feed, selection of suitable leaves should be driven by survival and fecundity of offspring, not by feeding 

preferences of adults as with many free-feeding insects. 

The leafminers differ from other endophagous insects, such as the stem and twig borers and 

gallformers, in several important ways. A leaf usually has less biomass than either a stem or a twig. 

Structurally, most leaves are essentially two-dimensional with little depth, while stems or twigs provide 

three-dimensional substrates. The two-dimensional nature of the leaf constrains the size and shape of 

larvae more than borers. Leafminers are the smallest of all the microlepidopterans and many are 

compressed dorso-ventrally. The lack of depth in leaves increases the likelihood of inter- and 

intraspecific interactions and may facilitate attack by natural enemies. Leaves are generally more 

photosynthetically active and composed of different cell types than twigs or stems. Some galling insects 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

219 
are also confined to feeding on single leaves, but by virtue of their isolating properties, galling insects 

are less likely to interact directly with other galling insects. Gall tissues also differ phytochemically 

from the leaves in which they are formed (Zucker 1982). Thus leafminers may be more intimately 

associated with their host leaves than are gallformers. 

I contend that this close association between leafminers and the leaf substrate causes 

phenological and morphological traits of plants to override other factors in governing host plant 

resistance. The biology and ecology of a lepidopteran leafminer, Cameraria sp. nov. Davis 

(Lepidoptera: Gracillariidae, agrifoliella group), are presented to elucidate that argument. 

HOST PLANT RESISTANCE 

Strictly speaking, plant resistance consists of the intrinsic (inherited) traits of a plant which 

prevent herbivore damage (Williams et al. 1988). Many extrinsic factors, however, such as abiotic 

conditions, interactions with natural enemies and other herbivores (including microbes), and the 

association of the host plant with other plants, influence the susceptibility of host plants to insect 

herbivores. Here, resistance is considered in the broad sense, i.e. what factors generally influence 

abundances, and thus population dynamics, of leafminers on their host plants. 

Temporal and Spatial Patterns 

of Abundances of Cameraria on Emory Oak 

Cameraria sp. nov. Davis is a dominant, univoltine leafminer on Quercus emoryi (Fagaceae) in 

some localities in central Arizona. Adults emerge from puparia inside leaves as they abscise in April. 

Adults mate and females oviposit on newly expanded leaves in late April to early May. Eggs hatch a 

few days after oviposition and larvae immediately form upper-surface, blotch mines. Larvae complete 

three to four instars by August to September, apparently undergo a larval diapause in winter months 

(although larvae can be observed feeding on warmer winter days), then rapidly complete the last four 

to five instars in March and April, and pupate in leaves to complete the yearly cycle. Successful larvae 

consume most of the upper-surface leaf area of the relatively small Emory oak leaves (Bultman and 

Faeth 1986a ). 

I have monitored the temporal patterns of abundances of Cameraria on eight Emory oak trees 

at a locality in central Arizona (Oak Flat, Pinal Co.) noted for unusually high densities. Other 

leafmining species typically remain at very low densities (= 1 mine/100 leaves) on Emory (Faeth 1986) 

and other oaks (Faeth and Simberloff 1981 ). Several spatio-temporal patterns emerge. Resistant trees 

in one season tend to be resistant in the next (Fig. 1a, 1b) and whereas overall abundances vary among 

trees and years, the pattern of tree resistance remains the same, as does the pattern of higher densities 

within trees on interior, shaded leaves (Fig. 2). 

Patterns of spatial distribution at finer scales have also been observed. Within trees, Cameraria 

is highly clumped among leaves (Faeth 1990). Fewer unmined leaves and more leaves with more than 

two mines occur than would be expected by chance. The leafminer occupies larger leaves more 

frequently than small ones. Within leaves, multiple mines are clumped on the basal half of individual 

leaves (Faeth 1990). 

Two related questions emerge: what factors determine the pattern of among-tree distribution, 

and how are the consequences of within-tree and within-leaf clumping of Cameraria related to this 

pattern? Both of these questions are fundamental to concepts of plant resistance. The first examines 

the initial colonization or habitat selection of trees and leaves, which is a function of female 

oviposition choice. The second question focuses on the fate of the population after colonization and 

thus on future colonization by leafmining survivors. 

220 
CJ 1985 ~1986 SUN LEAVES 

.. 1987 IZZJ 1988 1 A ~ 7 

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A 8 c D E F G H 

TREE 

Figure 1. Relative resistance of sunny (lA) and shaded (lB) regions within 

eight study trees to Cameraria infestation over four growing seasons. 

Resistance is defined as rank by mean density. Ranks of sun and shade leaves 

in one season were tested for independence in the following season by 

Kendall's nonparametric test for independence and are as follows: 

Sun, 1985-86, p > 0.20; 1986-87, p < 0.001; 1987-88, p > 0.40; Shade, 

1985-86, p < 0.001; 1986-87, p < 0.001; 1987-88, p- 0.05. Densities of Tree 

H were not recorded in 1985. 

221 
....--... 

(./) 

w 

~ w 

_J 

0 

0 

~ 

w 

0... 

(/) 

w 

z 

~ 

~ (./) 

z 

w 

0 

140 

120 

100 

80 

60 

40 

20 

0 

e-eSHADE 

0-0SUN 

1985 1986 1987 1988 

YEAR 

Figure 2. Mean densities of Cameraria (± SE) in sun and shade leaves from 

1985 to 1988. Densities in shade leaves are significantly greater than sun 

leaves in each year, except 1985 (paired t-test, 1985, t- 2.23, df- 6, 

0.10 > p > 0.05; 1986, t- 4.92, df- 7, p < 0.01; 1987, t- 4.53, df- 7, 

p < 0.01; 1988, t- 2.40, df- 7, p < 0.05). 

Oviposition Choice 

The operation of selection on adult females via survival of offspring has apparently resulted in 

behavioral and physiological mechanisms by which they discriminate suitable leaves for oviposition, at 

least in some leafminers. McNeil and Quiring (1983) reported an oviposition deterring pheromone in 

the dipteran alfalfa blotch miner, and others have suggested that lepidopteran leafminers can detect the 

presence of conspecific eggs (Simberloff and Stiling 1988, Auerbach and Simberloff 1989). In all of 

these studies, co-occurrence with conspecifics on a leaf resulted in increased mortality. Godfray (1986) 

showed that observed clutch size (three per leaf) of the leafmining fly, Pegomyza nigrotarsis, produced 

greatest larval survival, suggesting that natural selection has optimized clutch size. In addition to the 

presence of conspecifics, adult leafminers select leaves based on phenological or morphological traits 

such as 1) leaf size (Bultman and Faeth 1986a, 1986d, Godfray 1986, Faeth 1990), 2) propensity of 

leaves to abscise (Bultman and Faeth 1986c, Stiling et al. 1987, Simberloff and Stiling 1988), 

3) previous leaf damage (Faeth 1986), and 4) age of leaves (Quiring and McNeil 1987). 

222 
Budbreak phenology can also influence oviposition and, consequently, densities. Some 

leafmining species embed eggs only on new, supple leaves, perhaps because the ovipositor cannot 

penetrate mature, toughened leaves. Auerbach and Simberloff (1985) showed that atypical production 

of new, secondary leaves on Quercus nigra resulted in increased densities of two leafmining species that 

are restricted to oviposit and feed on new foliage. Opler (1974) suggested that late-season generations 

of the leafminer Neurobathra bohartiella, a new leaf specialist, were dependent on early-season 

defoliations by a dioptid moth that resulted in secondary flushing of new leaves. 

It is interesting to note that all of the above features associated with habitat selection are 

pheromonal, phenological, or morphological, and not phytochemical. Phenological and morphological 

features of leaves and detection of the presence of co-occurring leafminers may be more important 

than phytochemistry in determining habitat selection by females. Possible reasons for the absence of 

correlation of habitat selection and larval survival with phytochemistry are discussed below. 

Population· Dynamics 

Once the feeding substrate has been more or less fixed via oviposition, do factors which 

influence survival of larval leafminers differ from those which affect free-feeding insects? 

Abiotic Factors 

Feeding within leaves may ameliorate certain abiotic factors known to affect free-feeding 

folivorous insects. Because of insulation provided by the leaf, larvae may be less susceptible to external 

temperature fluctuations. Some species of leafminers continue to feed on evergreen host plants during 

the winter months in temperate zones despite sub-freezing external temperatures that kill externallyfeeding larvae. In some cases, the translucent mine may act as a miniature greenhouse, since domeshaped blotch mines may magnify sunlight (Hering 1951). 

In warmer climates, leafminers continue to feed when external temperatures rise above lethal 

limits for most externally-feeding insects, perhaps due to the mine's insulation and cooling provided by 

evapo-transpiration from stomata. Leafmining larvae are less susceptible to desiccation since the 

environs of the mine provide higher relative humidity than ambient air (Hering 1951). Cameraria's 

unusually long larval development time (11 months) in Arizona, which includes both extremely warm 

and sub-freezing temperatures, may be possible due to the amelioration of harsh ambient temperatures. 

Opler (1974) proposed that leafminers feed longer on evergreen oaks than deciduous ones because of 

poorer leaf quality. I suggest that these long development times are not caused by phytochemistry, but 

rather that internal feeding negates many of the climatic hazards of feeding externally. In addition, 

prolonged development in the case of Cameraria appears to reduce attack by predators. The larvae 

escape ant predation (see discussion of natural enemies below) by remaining small during the summer 

months when ant activity is greatest and rapidly growing in late winter to early spring when ant activity 

is low (Faeth, unpubl. data). 

Host Plant Factors 

Phytochemistry. One might hypothesize that phytochemistry is a crucial factor in survival of leafminers 

because of their confinement to individual leaves. Variation in phytochemistry is a prevalent 

explanation for non-random distribution of free-feeding insects (Denno and McClure 1983~ Kareiva 

1983, Spencer 1988). However, studies of leafminers have usually shown that phytochemistry is either 

not related to leafminer abundances or shows an inverse relation to that predicted (Feeny 1970, Faeth 

et al. 1981a, Faeth 1985, Stiling et al. 1982, Bultman and Faeth 1988, Rooney 1989). Similarly, in a 

detailed study of nutritional (protein) and allelochemical (tannin) variation among and within trees, the 

distribution of Cameraria among or within trees was not correlated with any phytochemical parameters 

223 
(Faeth 1990). Moreover, survival of Cameraria larvae was not related to phytochemical parameters of 

individual leaves (Faeth 1990). 

The general failure of phytochemistry to explain host plant resistance to leafminers may be 

accounted for in several ways. First, leafminers, like other endophagous insects, are more specialized 

on host plants (narrower host ranges) than insects that feed externally (Hering 1951, Powell 1980, 

D. Tonkyn, pers. comm.) and therefore may be better physiologically and behaviorally adapted to the 

chemistry of their host plants. However, performance of specialized insects is not necessarily better on 

their host plants than that of generalists (Bernays and Graham 1988). Second, specialized feeding 

within leaves by leafminers may circumvent poor quality tissues. Some larvae feed only on selected 

tissue layers that may be more nutritious and contain lower amounts of fiber and secondary compounds 

(Needham et al. 1928, Hering 1951). However, some leafminers feed primarily on tissue layers that 

contain secondary compounds (e.g. palisade layers), and others mine fully through all depths of the leaf 

such that ingestion of some tissues with secondary compounds is certain. Third, other phenological 

and morphological features of leaves may override differences in chemistry. This explanation seems 

most likely. Although phytochemical cues may play some role in the location of adult females of 

appropriate host plants and leaves within host plants, phytochemical effects on offspring may be less 

important than phenological and morphological ones. Furthermore, effects of morphology and 

phenology may interact with effects of competition and natural enemies. 

Phenology and morphology. The link betweel) oviposition choice and offspring survival is most evident 

when host plant phenology and morphology are considered. Endophagism increases risks of larval 

death from early leaf abscission via desiccation (Askew and Shaw 1979a, Faeth et al. 1981b, Williams 

and Whitham 1986, Stiling et al. 1987, but see Kahn and Cornell 1983, Pritchard and James 1984), and 

adults of some species may select leaves within trees based on propensity to abscise (Bultman and 

Faeth 1986c, Stiling et al. 1987, Simberloff and Stiling 1988). The effect of leaf abscission varies 

greatly depending on length and seasonality of larval development, leaf area required by larvae, normal 

leaf duration (i.e. deciduous versus evergreen), and external climatic conditions (early abscission in hot 

and dry locales may exacerbate desiccation) (Bultman and Faeth 1986c). 

Variation in budbreak phenology can directly affect abundances of leafminers via availability of 

leaves for oviposition, but variable budbreak can also indirectly affect larval mortality. Variation in 

budbreak leads to differences in ages of leaves which can affect survival, often in complex ways. For 

example, West (1985) forced oviposition on young, spring leaves by a leafminer that normally oviposits 

on mature leaves and found that survival on young leaves declined due to interactions with chewing 

folivores that prefer new leaves. Quiring and McNeil (1987) showed that the dipteran leafminer, 

Agromyza frontella, preferentially searched and oviposited on new leaflets of alfalfa, but apparently 

because these leaves were less likely to be occupied by conspecifics. A late-season Cameraria sp. nov. 

(guttifinitella group), which normally mines mature leaves of Emory oak, will oviposit on new, secondary 

foliage. Survival is higher in new foliage than mature foliage because these leaves are less likely to 

abscise than mature leaves (Faeth 1987). 

Leaf size can strongly affect larval survival and fecundity, particularly for leafminers that require 

relatively large areas of leaves for successful development (Bultman and Faeth 1986d). Bultman and 

Faeth (1986a) showed that four species of leafminers on Emory oak chose leaves for oviposition 

according to leaf area required for larval development (i.e. leafminers requiring small areas chose small 

leaves and those requiring large areas chose large leaves). However, leaf size was correlated with 

survival only for Cameraria sp., which requires large leaf areas. 

Natural Enemies 

Hering (1951) proposed that feeding within mines kept leafminers protected from natural 

enemies. Powell (1980) implied that endophagous lepidopterans have not evolved characteristics that 

permit exposed feeding (distastefulness, urticating hairs and glands, aposematism) because endophagism 

224 
provides protection from natural enemies. Among-guild comparisons are difficult, but apparently 

natural enemies of leafminers are neither less diverse nor is attack on them less intense than that on 

free-feeding insects. Invariably, detailed studies of leafminers reveal a wide array of parasitoid species 

attacking each leafminer species (Askew and Shaw 1974, 1979a, 1979b, Green 1979, Hawkins 1988, 

Faeth sub. man.). Moreover, natural enemies (parasitoids and predators) typically account for a large 

fraction, if not the majority, of the mortality of leafmining larvae and pupae (Askew and Shaw 1979a). 

Many parasitoid species specialize on certain leafmining species by using cues associated with the mine 

or frass (Hawkins 1988) or even acoustic signals of mining larvae (Sugimoto et al. 1988). At present, 

then, there is no evidence to suggest that leafminers are more protected from natural enemies than are 

other herbivorous insects. 

At least in some cases, however, the opposite may be true. Gross and Price (1988) found that 

an obligate gelechiid leafminer on horsenettle is more vulnerable to macroparasite attack than a 

congeneric facultative leafminer on groundcherry that can depart the mine and move freely over the 

leaf surface. The horsenettle trichome morphology apparently has selected for mine architectures, 

which exclude free-feeding and, in tum, increase parasitism. Because of humid and perhaps warmer 

conditions within the mine, leafminers may also be more susceptible to infection by microbial parasites 

or pathogens such as fungi and bacteria (Faeth and Bultman 1986). 

Natural enemies of Cameraria include more than 20 species of Hymenoptera, mostly in the 

families Encyrtidae, Eulophidae, and Braconidae. Predators are mostly adult parasitoids, which feed on 

larvae, and the arboreal ant Pseudomyrmex apache. Typically, rates of natural enemy attack are from 

15 to 40 percent. Natural enemy attack varies among trees and within trees, probably as a function of 

leafminer .densities and local distribution of natural enemies (Faeth 1980), although not necessarily in a 

density-dependent fashion (Heads and Lawton 1983, Stiling 1987). 

Natural enemy attack may also be a complex function of interaction with other herbivores and 

the ensuing phytochemical and morphological changes they cause. Faeth (1986), for example, showed 

that leafminers feeding in leaves previously damaged either artificially or by herbivores had significantly 

increased rates of parasitism. Subsequent experiments indicated that both phytochemical (Faeth and 

Bultman 1986) and structural (Faeth, unpubl. data) changes induced by herbivory can increase the rate 

of natural enemy attack. 

Competition 

Confinement within leaves increases the probability of inter- and intra-guild interactions relative 

to other folivorous insects. The vagility of free-feeding insects permits behavioral avoidance of both 

direct (interference competition or cannibalism) and indirect competition as well as amensalistic 

interactions (exploitation competition, induced defenses, competition via natural enemies). Such is not 

the case for leafminers. Competition has been shown to occur for hymenopteran leafminers on birch 

trees (Tuomi et al. 1981), for dipteran leafminers on citrus (Murai 1974), alfalfa (Quiring and McNeil 

(1984), Spartina (Stiling et al. 1984), and American holly (Potter 1985), and for lepidopteran leafminers 

on oak (Bultman and Faeth 1986b, Auerbach and Simberloff 1989). Cannibalism or killing of cooccurring conspecifics (Condrashoff 1964, Murai 1974, Quiring and McNeil 1984, Auerbach and 

Simberloff 1989, Faeth 1990) is probably more common among leafminers than free-feeding folivores at 

comparable densities because of restriction within leaves. 

The sedentary nature of leafminers also increases susceptibility to amensalistic interactions with 

nonleafmining insects. Punctures or tears in mines via feeding by leafchewing or sucking insects can 

result in desiccation and death of most larval leafminers. Insect damage to nonmined areas of the leaf 

can increase the propensity of the leaf to abscise (Faeth et al. 1981b, Faeth 1986), change the 

phytochemistry of the leaf (Faeth 1986), attract natural enemies (Faeth and Bultman 1986, Faeth 

unpubl. ), and increase the likelihood of leaf infection by endophytic or epiphytic fungi (K. Hammon, 

225 
pers. comm.). Interactions with free-feeding insects are generally unilateral, since mining damage is 

usually minimal and can be avoided by mobile insects (but see Hartley and Lawton 1987). 

Morphological and phenological variation may influence the intensity of intraspecific competition. 

Competition among leafmining larvae should be a function of relative leaf size as well as density and 

dispersion of the leafmining larvae. A field study is described to illustrate the complex interactions of 

variation in leaf size with density, dispersion, and competition among Cameraria. 

EMORY OAK RESISTANCE TO CAMERARIA 

Methods 

To test the hypothesis that leaf size influences Cameraria colonization, dispersion, and 

subsequent survival via intraspecific interactions, 12 branches of Q. emoryi (two branches per six trees) 

were enclosed with fine mesh screening before budbreak in 1986. Twenty pupae were added to each 

enclosure on 24 April 1986, about a week after budbreak. Emerging adults were allowed to mate and 

oviposit on leaves within enclosures. Enclosures were removed at the first appearance of larval mines 

to allow access of natural enemies and to minimize any cage effects. All mined leaves were marked 

with a small dot of latex paint so that any abscised leaves could be identified (abscised leaves were 

collected from beneath trees bimonthly during the study period). Enclosures were again placed on the 

branches in late March 1987 to capture leaves during the peak of leaf abscission. Pupation and most 

natural enemy attack occur before this time. Leaves were collected from within enclosures on 3 and 

24 April 1987; all leaves had abscised from the branches by the latter date. 

Collected leaves were returned to the laboratory and each was examined for the presence and 

number of mines to determine densities and distribution. Distribution on each branch was tested 

against a random (Poisson) and, if significantly different, against a clumped (negative binomial) 

distribution. Densities were plotted against k of the negative binomial to determine the relationship of 

density and degree of clumping. Sizes of mined and unmined leaves were determined by weighing a 

random sample of dried leaves in each category from each branch. 

Survival (presence of an emergence hole or protruding pupal case) or mortality of each 

leafminer was ascertained by dissecting each mine. Specific categories of mortality were not ascertained 

for dead leafminers. Thus I examined intraspecific competition in the broad sense, i.e. how cooccurrence affects overall mortality, be it from cannibalism, depletion of food resources, increased leaf 

abscission, or changes in rates of natural enemy attack. The question of interest in this study is how 

leaf size and densities interact to affect survival and thus population dynamics and tree resistance. 

Other studies in this system have examined specific categories of mortality in detail (Bultman and 

Faeth 1986b, 1988, Faeth and Bultman 1986, Faeth 1990). 

To test for density-dependent effects at the spatial level of the branch, survival of all leafminers, 

of leafminers occurring alone, of those co-occurring with one conspecific, and of those co-occurring 

with two or more conspecifics were regressed separately against mean branch densities. 

Because of leafminers' confinement within leaves, tests of density-dependent mortality of 

leafminers may be more appropriate at finer spatial scales (i.e. within leaves of varying sizes with 

varying numbers of co-occurring leafminers). Log linear analysis was therefore used to determine 

relationships between the response variable, survival (S), and leaf size (L), number of mines per leaf 

(M), and aggregation within branches (K), estimated by k of the negative binomial. Plots of k versus 

branch densities showed that branches fell into two categories: low and high degree of clumping 

(Fig. 3). Leaf sizes were divided into three categories: small (0-30 mg dry mass), medium (31-60 mg) 

and large ( > 60 mg) leaves. Categories of mines per leaf were one, two, and > two per leaf. The 

226 
3.0 

~ 2.5- __, 

<( 

2 

0 2.0-

z 

m 

w 1 .5- > 

~ (.!) 

w 1 .0-

z ......._., 

..!:L. 0.5-

0.0 

0.0 

• 

0 HIGH DENSilY 

e LOW DENSilY 

• • • 

0 

0 

0 

0 

0 0 

I I 

0.5 1.0 

DENSITY (MINES PER LEAF) 

0 

Figure 3. Relationship of density of Cameraria and k of the negative 

binomial. 

0 

response variable, survival, was simply whether each leafminer in each multi-way classification had 

either survived or died. 

1.5 

Log linear analysis is a powerful method of examining relationships among categorical variables 

(Jenkins 1975, Veps!Utinen et al. 1988), but it is subject to certain statistical and biological 

assumptions. I followed the methods of Jenkins (1975) by beginning with the most complex model (all 

four three-way interactions) and then testing progressively simpler models (dropping complex 

interaction terms) until the simplest model was found where the log-likelihood ratio was no longer 

significant at p s .05. This method assumes that the simplest model is the most biologically relevant 

one (Jenkins 1975). Data was partitioned in a biologically reasonable fashion based upon previous 

studies and knowledge of the system. Data was combined from all branches so that cells within the 

multi-way table were sufficiently large (Veps!l!inen et al. 1988). 

Results 

Dispersion 

Dispersion of leafminers on all branches was significantly different from a random Poisson 

distribution (Table 1). Generally, more leaves were unmined and more leaves had multiple mines than 

would be expected by chance. On nine of the 12 branches, dispersions were not significantly different 

from that expected by a negative binomial (clumped) distribution (Table 1 ). Leafminers were also 

more aggregated (smaller k) at lower densities than higher ones (Fig. 3). 

227 
Table 1. Spatial distribution of Cameraria among leaves within individual 

branches compared to a random (Poisson) and an aggregated (negative 

binomial) distribution. Common letters denote branches from the same 

tree. Chi square tests of significance are based upon deviation of 

observed from expected. Observed classes with < 5 observations are 

lumped with previous categories. Number of classes ranged from three 

(0, 1, > 1 mines per leaf) to seven (0, 1, 2, 3, 4, 5, > 5 mines per 

leaf). 

Branch p@ 

Chi square Poisson Chi square Negative binomial p@ 

lA 82.5 *** 0.2 NS 

2A 249.8 *** 12.1 * 

1B 161.4 *** 4.7 NS 

2B 258.8 *** 6.0 NS 

1C 65.4 *** 8.8 NS 

2C 183.3 *** 20.8 ** 

lD 155.0 *** 7.0 NS 

2D 49.7 *** 4.0 NS 

lE 39.2 *** 1.9 NS 

2E 96.8 *** 13.4 * 

lF 41.1 *** 1.2 NS 

2F 279.8 *** 7.9 NS 

@ NS, not significantly different; *, p < 0.05; **, p < 0.01; ***, p < 0.001. 

Leaf size 

For all branches, mined leaves were significantly larger than unmined ones (Table 2). 

Mortality 

Mortality was shown to be inversely related to density at the spatial scale of branches whether 

one considers overall mortality (Fig. 4a) or mortality of leafminers occurring alone (Fig. 4b ), with one 

conspecific (Fig. 4c), or with more than two conspecifics (Fig. 4d). 

At the finer spatial scale of individual leaves, the simplest log linear relating survival (S) to 

clumping (K), leaf size (L ), and mines per leaf (M) is: (LK)(LM)(SK)(SM). Inclusion of three-way 

interactions did not improve the model, nor did inclusion of the two other possible two-way 

interactions, (SL) and (KM). This model suggests that degree of branch clumping and number of 

mines per leaf are related to leaf size ((LK) and (LM) terms). Generally, more single mines and fewer 

multiple mines occurred on small leaves as compared to medium or large leaves (Fig. 5). Survival was 

a function of degree of clumping both at the level of the branch (SK term) (Fig. 6) and at the level of 

individual leaves (SM term) (Fig. 6). Under conditions of high branch clumping, survival was lower for 

leafminers occurring alone or with other oonspecifics (Fig. 6). Finally, branch clumping was shown to 

228 
100 1986-1987 ~ Z flit R 2 - .57 :i 90 ••••• - . . • •.... 

-i ........ ·• • 3. 80 flit ....... . 

>- • • • 1- 70 

~ ~ 60 :::::& 

~ 50 

o 4 A ffi 40 n. 30+---~--~--~ . .---r---.---~.---..~ 

0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 

BRANCH DENSilY (MINES PER LEAF) 

~ 100 

~ 90 ••••• - • • • flit 

1986-1987 

R 2 -.58 

• e •........ ~ .... • ~ 80 • , ...... . 

~ 70 • • 

~ 60 :::::& 

~ 50 0 15 40 4C n. 

30+' --~-----~~--~--~--~--~---.~ o.o 0.2 0.4 0.6 0.8 1.0 1.2 1.4 

BRANCH DENSilY (MINES PER LEAF) 

'W 100 

~ 90 

~ 

- 80 ~ 

~ 70 ~ 

g 60 

~ 50 0 

ffi 40 n. 

• 

48 

• .•.. • 

. ·• 

• 

• 

1986-1987 

R 2 - .7J 

• 

• 

• •••• 

~+.o---o~.-2---0 •. 4---0T.s---o~.-8---,·.o---,T .. 2---.,-4~ 

BRANCH DENSilY (MINES PER LEAF) 

~ 100 

~ 90 

c 80 

~ 70 

~ ~ 60· :::::& 

~ 50 

0 40 ffi 

n. 

flit 1886-1887 

... .. . . .... .. .. . 

.............. . . . 

• 

R 2 .... 45 

40 

30+---~---r--~---.----r---.-.--~~ 

0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 

BRANCH DENSilY (MINES PER LEAF) 

Figure 4. Regressions of mean branch density and mortality for all leafminers 

pooled (4A), those occupying leaves alone (4B), with one conspecific (4C), or 

with more than one conspecific (4D). All slopes of regressions are 

significantly different from zero (p < 0.05). 

be a function of available leaf sizes (LK term), and more clumping occurs when mean leaf sizes of 

branches are small (Fig. 7). Of interest is that the term (SL) is not in the model. Survival was not a 

function of leaf size (Fig. 8), although adults apparently oviposit more frequently on larger leaves 

(Table 2). 

DISCUSSION 

Contrary to expectations, mortality of Camerari.a sp. nov. appears to be inversely densitydependent, at least at the spatial scale of branches (Fig. 4a-4d). This relationship is most pronounced 

for leafminers occurring alone (Fig. 4b ). Given this result alone, one might conclude that intraspecific 

competition is not an important process in the population dynamics of this leafminer. Others (Strong 

et al. 1984, Lawton and MacGarvin 1986) have concluded on the basis of evidence from insect life 

tables that population dynamics of phytophagous insect populations are generally not driven by 

competition. 

However, consideration of mortality only at the level of branches may obscure the complex 

interactions underlying the dynamics of Camerari.a. The more appropriate scale may be that of the leaf 

because, after all, that is where ultimate oviposition choice and larval-larval interactions occur. When 

229 
Table 2. Mean size in mg (± SE) of all (mined and unmined leaves) and mined 

leaves. Sample sizes of each category for each branch are in 

parentheses. 

Mean size of all leaves Mean size of mined leaves 

Branch Mean ± SE (N) Mean ± SE (N) 

lA 26.24 ± 11.28 (50) 36.24 + 10.18*** (41) 

2A 27.46 ± 12.26 (50) 40.95 ± 13.26*** (99) 

lB 32.75 ± 16.01 (50) 44.61 + 16.47*** (99) 

2B 34.00 ± 16.71 (50) 48.98 ± 18.97*** (122) 

lC 38.69 ± 19.49 (50) 45.90 + 16.10** (125) 

2C 42.71 ± 19.49 (50) 51.20 ± 17.56** (172) 

10 48.63 ± 20.39 (50) 58.85 ± 19.30** (77) 

20 38.98 ± 18.57 (50) 49.72 ± 14.01*** (132) 

lE 40.57 ± 19.64 (50) 52.44 ± 18.oo*** (151) 

2E 38.17 ± 21.71 (50) 55.29 ± 19.88*** (147) 

1F 38.97 ± 19.21 (50) 48.69 ± 19.81** (126) 

2F 37.68 ± 16.48 (50) 48.76 ± 15.17*** (170) 

** Significantly different mean size of mined leaves compared to mean size of 

all leaves by Student's t test at p < 0.01 

*** Significantly different mean size of mined leaves compared to mean size of 

all leaves by Student's t test at p < 0.001 

one considers mortality at the level of leaves, a different picture emerges. Survival is a function of 

number of mines per leaf. Most of this increase in mortality (and decrease in pupal mass, and thus 

fecundity, of survivors) with mine number is attributable to cannibalism, and, secondarily, to premature 

leaf abscission (Faeth 1990). Translated into the spatial scale of branches, survival becomes a function 

of how clumped larvae are, with greater clumping leading to decreased survival (Fig. 6). Oearly, 

Cameraria mortality ~ density-dependent, but only when one examines the proper spatial scale. 

I propose that Emory oak resistance to Cameraria is based in part on variation in leaf sizes, 

which influences the two components of tree resistance, colonization by ovipositing females and survival 

of larval offspring. At the level of the branch, clumping appears to be a function of available leaf 

sizes (LK term) (Fig. 7), with mean leaf size of the branches explaining a significant (R2 = 0.43) 

proportion of the variation in k, an index of clumping. At the scale of individual leaves, number of 

mines per leaf is also related to leaf size (LM term). Rejection of small-sized leaves for oviposition 

(Table 2) is the likely mechanism for clumping within branches and among leaves (Faeth 1990). 

Rejection of small leaves may be selected through survival of offspring. A larva requires relatively 

large areas of Emory oak leaves successfully to complete development. Of the 1,915 mined leaves 

examined in this study, no leafminer survived in leaves of less than 20 mg dry mass. A critical lower 

size limit thus exists below which survival of even single leafminers does not occur. Thus branches or 

230 
>- (.) 

z 

w 

::::> 

CJ 

w 

0::: 

u... 

70 

60 

50 

40 

30 

20 

10 

CJ 1 MINE/LEAF 

~ 2 MINES/LEAF 

lZZI >2 MINES LEAF 

SMALL MEDIUM 

LEAF SIZE 

1986-87 

LARGE 

Figure 5. Percent of leafminers occurring on small-, medium- and large-sized 

leaves by number of mines per leaf. 

trees with smaller mean leaf sizes may be more resistant at oviposition because fewer eggs are laid and 

those that are tend to be highly clumped on the reduced pool of suitably sized leaves. The high degree 

of clumping suggests that these females do not have an oviposition deterring pheromone as do some 

other leafminers (McNeil and Quiring 1983, Simberloff and Stiling 1988, Auerbach and Simberloff 

1989), although this is yet to be determined. 

Increased clumping clearly results in increased larval mortality, the second component of tree 

resistance. Co-occurrence exacerbates cannibalism, exploitation competition, and premature leaf 

abscission. Leafminers in highly clumped branches have lower survival when occupying multiply or 

singly-mined leaves (Fig. 4a-4d). When survival in individual leaves was examined, only 25 of the 1,617 

multiply-mined leaves in this study had two larvae that survived simultaneously, and none had more 

than two. The consequences of confinement and co-occurrence in terms of intraspecific competition 

are thus severe. Colonization in the next growing season may be reduced and resistance thus 

reinforced if colonization occurs primarily in situ. Since pupation and emergence occur in leaves that 

have fallen beneath relatively isolated oak trees at the study site, this prediction may hold. 

Experiments are underway to test this hypothesis. 

In 1987 we tested leaf size as a predictor of resistance independently by correlating leafminer 

densities with mean leaf size on eight Emory oak trees. Mean leaf size is a good predictor of density 

and explains a significant proportion of the variation in densities (R 2 = 0.41) (Fig. 9). Considering 

the multifarious factors that can influence host plant resistance to insects, it is noteworthy that a 

single parameter, mean leaf size, can predict a large part of oak tree resistance to leafminers. 

231 
C) 

w 

> 

> 0:: 

::> 

(/) 

.._ 

z 

w 

(.) 

0:: 

w 

a_ 

60 

50 

40 

30 

20 

10 

0 

CJ 1 MINE/LEAF 

~ 2 MINES/LEAF 

lZZI >2 MINES LEAF 

HIGH LOW 

CLUMPING (GROUPED BY k) 

1986~87 

Figure 6. Survival of leafminers occurring alone, and with one or more 

conspecifics on branches grouped by high (n - 4) or low (n - 12) degree of 

branch clumping as indicated by k of the negative binomial. 

Certainly, leaf size does not explain all the variation in tree resistance to leafminers. Two other 

phenological factors, variation in premature leaf abscission and timing of budbreak, can also influence 

colonization and survival. For example, Bultman and Faeth (1986c) showed that leaf abscission rates 

are greater in sun leaves compared than leaves and can explain some variation in both distribution and 

mortality. Others (Askew and Shaw 1979a, Faeth et al. 1981b, Potter 1985, Stiling et al. 1987, 

Simberloff and Stiling 1988, Auerbach and Simberloff 1989) have shown that premature leaf abscission 

is an important factor in leafminer survival. Higher rates of premature leaf abscission for sun leaves 

(Bultman and Faeth 1986c) may explain why leaf size accounts for less variation in Cameraria densities 

on sunny than shaded leaves (Fig. 9) (sun leaves R 2 = 0.27, shade leaves R 2 = 0.51 ). 

Variable budbreak probably influences initial colonization also, since colonization is closely 

synchronized with budbreak. For example, unusually warm weather in the spring of 1988 caused early 

budbreak accompanied by emergence of leafmining adults. A late frost then occurred, many new leaves 

were destroyed, and further budbreak ceased on some trees until after adults had disappeared. These 

events may explain some reversals in tree resistance in 1988. Tree C, for example, exhibited delayed 

bud break, and resistance greatly increased in 1988 as compared to previous years (Fig. 1 ). Obviously, 

both variable budbreak and abscission may act to intensify intraspecific interactions if the pool of 

suitable leaves for oviposition is enlarged and increased clumping ensues. 

232 
2.0 

1 .8-

,--.... 1.6- ....J 

~ 

::IE 1.4-

0 

z 1 .2-

CD 

w 1 .0-

> 

~ 0.8-

(.!) 

w ·o.s- z 

"'-/ 

~ 0.4-

0.2-

0.0 

20.0 

1986-87 

~ORE CWMPED 

••• •• 

I • I 

25.0 30.0 

•• I 

35.0 

• • 

••• 

• 

I 

40.0 

MEAN LEAF SIZE (mg) 

2 R = .43 

LESS CLUMPED 

• 

• 

I 

45.0 50.0 

Figure 7. Relationship of clumping (k) and mean leaf size of individual 

branches. Slope of the regression is significantly different from zero 

(p < 0.05). 

It is important to note that neither foliar nutrition nor allelochemical variation, long the bastion 

for explaining resistance of host plants to phytophagous insects, appears to determine Emory oak 

resistance to Cameraria (Faeth 1990). This is not to say that phytochemistry is not important in adult 

selection of, or larval survival in, leaves. Leaf size, for example, probably co-varies with some 

phytochemical parameter used by ovipositing females. It does seem, however, that variable phenology 

overrides variable phytochemistry in the dynamics of this leafminer. 

It is premature to suggest that host plant resistance to other species of leafminers is driven 

mainly by phenological factors and their effects via competition. Leaf size, for example, may have little 

effect on leafmining species that require relatively small leaf areas for development or remain at low 

densities such that co-occurrence on leaves is rare. The latter situation is typical for most leafmining 

species, as it is for other guilds of phytophagous insects (Schultz 1983, Barbosa and Schultz 1987). A 

multitude of biotic and abiotic factors may be responsible for keeping populations of most 

phytophagous insects at low levels. I suggest, however, that the "ceiling" (sensu Strong 1986) on 

population densities of Cameraria and possibly other species in the leafmining guild is set by the 

interaction of phenological and morphological factors and competition. For example, in 1987, 

50 pupae were introduced into the same branch enclosures (2.5x the number introduced in 1986) in an 

effort to boost densities and thus interactions. Yet leafminer abundances were not different from those 

in 1986 (1986 x = 0.844 (± 0.37) mines/leaf, 1987 x = 0.986 (± 0.73) mines/leaf, paired t = 1.04, 

df = 11, and p > 0.20). Branches and trees may thus be saturated in this system, although many 

leaves were not mined because they were either 1) of unsuitable size, 2) likely to abscise, or 

233 
40 

0 30 w 

> 

> 

~ 

:::> 

lf) 20 .__ 

z 

w 

u 

~ 

w 

c.. 10 

[::J SMALL LEAVES 

~ MEDIUM LEAVES 

EZ1 LARGE LEAVES 

s M 

LEAF SIZE 

L 

1986-87 

Figure 8. Percent of leafminers surviving on small-, medium-, and largesized leaves. Data from leaves with varying numbers of mines per leaf were 

pooled. The interaction of leaf size and survival is not a significant term 

in the log linear model. 

3) unavailable for oviposition due to variable budbreak or time and energy constraints on female 

search. Saturation is further indicated in that leaf size per se, is not related to survival (Fig. 8). The 

risks of co-occurring with other conspecifics on larger leaves may be balanced by risks of mining alone 

on smaller leaves when densities are saturated. 

The "ceiling" on Cameraria populations may be much lower than expectations based upon simple 

density estimates, especially if one considers the relationship between density and mortality at the 

wrong spatial scale. Variation in phenology and morphology and search constraints on females may 

restrict the pool of high quality leaves such that competition occurs at relatively low densities. 

SUMMARY 

Leafminers are endophagous insects that spend all or part of their larval feeding stages confined 

within leaves. Oviposition thus determines larval feeding sites among and within host trees and leaves. 

Host tree resistance to leafminers may be a function of initial colonization via female ovipositional 

preferences and the way in which these preferences translate into survival of offspring. For leafminers, 

ovipositional choice and offspring survival may be more closely linked to variation in tree and leaf 

phenology and morphology than they are for free-feeding insects. 

234 
w 

N 

(/') 

Lt.. 

iS 

....J 

z 

iS 

~ 

100----------------------------------~ 2 

90· 

80· 

70-

60-

50-

e SUN LEAVES 

o SHADE LEAVES 

1986-87 

• 

• 

0 

... . . . . . . 40 ... ~. .• .•..... 0 0 

30- • • 

0 

20-

. .. 

0 

• ... ... . . . ... . .. 

0 

R = .41 

... . . . . . . 0 ... 

104-----~.----~.----~.----~.----~.----~.----~.----~.r-----r-.-

o.o 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 1.8 

DENSITY (MINES PER LEAF) 

Figure 9. Regression of mean size against density of Cameraria on sun and 

shade leaves from eight Emory oak trees. Slope of the overall regression (sun 

and shade data combined) is significantly different from zero (p < 0.05). 

To illustrate these arguments, patterns of abundances and distribution of a dominant leafminer, 

Cameraritl sp. nov., on Quercus emotyi are described. These patterns appear to be determined mostly 

by variation in leaf sizes among and within trees, which in tum causes variation in intensity of 

intraspecific competition among ovipositing females and their larval offspring. 

ACKNOWLEDGMENTS 

I wish to thank B. Axelrod, K. Bigelow, P. Cheng, T.J. Faeth, C. Febus, K. Hammon, S. Reeser, 

and R. Rooney for their assistance in the field or laboratory portions of this research. K. Hammon 

and R. Rooney offered helpful comments on the manuscript. This research was supported by NSF 

grants BSR 8415616 and 8715743. 

LITERATURE CITED 

ASKEW, R.R. and SHAW, M.R. 1974. An account of the Chalcidoidea (Hymenoptera) parasitising 

leaf-mining insects of deciduous trees in Britain. Biol. J. Linn. Soc. 6: 289-335. 

235 
ASKEW, R.R. and SHAW, M.R. 1979a. Mortality factors affecting the leaf-mining stages of 

Phyllonorycter (Lepidoptera: Gracillariidae) on oak and birch. I. Analysis of the mortality factors. 

Zool. J. Linn. Soc. 67: 31-49. 

ASKEW, R.R. and SHAW, M.R. 1979b. Mortality factors affecting the leaf-mining stages of 

Phyllonorycter (Lepidoptera: Gracillariidae) on oak and birch. II. Biology of the parasite species. 

Zool. J. Linn. Soc. 67: 51-64. 

AUERBACH, M.J. and SIMBERLOFF, D. 1985. Responses of leaf miners to atypical leaf production 

patterns. Ecol. Entomol. 9: 361-367. 

AUERBACH, M.J. and SIMBERLOFF, D. 1989. Oviposition site preference and larval mortality in a 

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BARBOSA, P. and SCHULTZ, J.C., eds. 1987. Insect Outbreaks. Academic Press, San Diego, CA 

578 p. 

BERNA YS, E. and GRAHAM, M. 1988. On the evolution of host specificity in phytophagous 

arthropods. Ecology 69: 886-892. 

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(Fagaceae). Oikos 46: 311-316. 

BULTMAN, T.L. and FAETH, S.H. 1986b. Experimental evidence for intraspecific competition in a 

leaf-mining insect, Cameraria sp. nov. (Lepidoptera: Gracillariidae). Ecology 67: 442-448. 

BULTMAN, T.L. and FAETH, S.H. 1986c. Selective oviposition by a leaf miner in response to 

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31: 210-206. 

BULTMAN, T.L. and FAETH, S.H. 1988. Abundance and mortality of leaf miners on artificially 

shaded Emory oak. Ecol. Entomol. 13: 131-142. 

CONDRASHOFF, S.F. 1964. Bionomics of the aspen leaf miner, Phyllocnistis populie//a Cham. 

(Lepidoptera: Gracillariidae). Can. Entomol. 96: 857-874. 

DENNO, R.F. and McCLURE, M.S., eds. 1983. Variable Plants and Herbivores in Natural and 

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FAETH, S.H. 1980. Invertebrate predation of leaf-miners at low densities. Ecol. Entomol. 5: 111-114. 

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239 
THE WITHIN-TREE DISTRIBUTION 

OF CATERPILLAR MINES 

MICHAIL V. KOZLOV and YULIA G. KORICHEVA 

All-Union Research Institute of Plant Protection 

Pushkin 8, Leningrad 189620 U.S.S.R. 

INTRODUCTION 

Lepidoptera is a relatively young order and one of the largest and most diverse in the Insecta. 

The first paleontological vestiges of moths were found among lower Jurassic deposits, but the most 

intensive lepidopterous evolution (mainly in suborder Ditrysia = Papilionina) took place in the midCretaceous Period, coterminous with the expansion of angiosperm plants. The flowering plants were a 

highly determinant factor in the development of the environment, their influence on moth speciation 

extending beyond provision of food for caterpillars and adults. The greatly increasing heterogeneity of 

plants in space and time became a base for many potential ecological niches, many of which were 

afterwards occupied by lepidopterous species. Paleontological data indicate that the mining mode of 

life was already formed in the first stages of lepidopterous evolution (Kozlov 1988). In recent time, 

mining caterpillars can be found in nearly all large groups of Lepidoptera. The mining moths are the 

most specialized ecological group, characterized by important morphological and physiological 

adaptations at larval stages. They interact very closely with their host plants. Applicability of the term 

"parasitism" to the mining moths is now under discussion: some authors consider all insects feeding on 

living plants to be parasites; others question the value of so broad a use of the term. Dogel (1962) 

wrote, "The parasites are organisms which use other living beings as environment and source of food 

and make their hosts responsible (partly or completely) for regulation of their interactions with 

external space." In line with this definition, we consider mining insects true parasites on their host 

plants. 

In this paper, we consider the question how mining caterpillar distribution on host plants 

reflects topical aspects of the coevolution of insects and plants. 

The Heterogeneity of Different Plant Parts and Their Influence on Herbivorous Insects 

Leaves on annual shoots differ in morphological, anatomical, and biochemical aspects. This 

phenomenon is called heterophylly (Serebryakov 1962). Important changes in leaf anatomical structure 

on annual shoots were described for the first time in Zalensky's (1904) classic work on more than 

40 plant species. Apical leaves of all studied plant species are more xeromorphic than basal ones: 

they have more ribs per surface unit, smaller epidermal cells, smaller mesophyllic cell diameters, thicker 

epidermal cell membranes, and more developed mechanical tissues. 

Krenke (1940) attributed heterophylly to the ontogenetic origin of leaves from structures of 

different ages. He established the cyclic character of metameric variability: the complete cycle can be 

described by the unimodal convex curve. This curve reflects changes in morphological and anatomical 

BARANCHIKOV, Y.N., MATfSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

240 
characteristics (leaf size, for example) and physiological processes, but serves only as theoretical 

background for the primary changes occurring with age. The majority of physiological processes, taking 

place during the ontogeny of each organ and plant as a whole, follow the unimodal curve; the length 

of its parts and the maximal point are different for various processes (Gupalo 1975, Klyachko and 

Kulaeva 1975). 

Analyzing the annual shoot structure of Liriodendron tulipifera, Vasiliev and Goltsova (1979, 

1980) distinguished six characteristic groups by the type of curve describing their changes. They 

stressed that the variability of external leaf characteristics is more pronounced than that of internal 

ones. The diversity of organ characteristics is greater than that of tissues and cells. 

The structure of a leaf depends both on its location on a shoot and the type of shoot. For 

example, the leaves of Populus alba short shoots are similar to the leaves on the base of the long ones 

(Pautov 1989). The peculiarities of leaves on different types of shoots are determined not by the 

differences in the structure of their growing apexes, but by development conditions. 

Leaf structure may be affected by environmental factors as well. Zalensky (1904), for example, 

showed that xeromorphic features increase in leaves as one moves from the basal to the top parts of a 

shoot. 

Initiation of different leaf elements in the bud does not take place not simultaneously. 

Accordingly, one can distinguish leaf parts different in age and different, therefore, in anatomical, 

morphological, and biochemical features. Basal and apical parts of a long leaf are known to be 

distinguished in the same way as basal and apical leaves on the shoot (Tshizhevskaya 1954). 

Thus we may conclude that both different leaf parts and different leaves on a shoot are 

distinguishable by anatomical, morphological, and biochemical features, which may determine their 

suitability for herbivorous insects. Let us consider, then, the ability of insects to distinguish specific 

leaf characteristics. 

One of the first reports on the ability of females to evaluate the size of host plant leaves 

demonstrated that egg clutch size of the lilac moth, Caloptilia syringella F. (Polejaev 1939), was 

positively correlated with leaf size. Similar results were obtained for the mining moths inhabiting oak 

Quercus emoryi (Bultman and Faeth 1986b) and for larvae of the mining fly, Pegomyia nigritarsis Zett., 

feeding on different Rumex species (Godfray 1986). The importance of this phenomenon promoting 

optimal food utilization is obvious, but its mechanisms are still unknown. Leaf preference of attelabid 

beetles, on the other hand, is determined by length of the leaf margin which the female runs along 

(Sakurai 1988a, 1988b ). 

The ability of the papilionid butterfly, Battus philenor L, to distinguish leaf shape has also been 

described. Females of this species prefer to lay eggs either on the wide-leaved Aristolochia reticulata or 

on the narrow-leaved A. serpentaria, depending on their individual experience. The leading role of 

vision in this process is confirmed by the fact that these females also visit nonhost plants with either 

wide or narrow leaves (Rausher and Papaj 1983, Papaj 1986). 

The female orientation to the color of the host plant leaf has been described for the fly, 

Pegomyia hyoscyami Panz., which lays its eggs on the dark, oldest leaves of beets. Leaf color in 

autumn is the chief criterion in choice of host trees by migrating female aphids Periphyllus californiensis 

Shinji: the majority of females prefer yellow-orange leaves, some of them prefer red, and all ignore 

yellow-green and green leaves. The species of the host plant, Acer amoenum or A. palmatum, is not a 

factor in the choice (Furuta 1986). 

The shape and color of leaves are usually distinguished by the insects remotely. Any additional 

information about plant chemistry and its surface structure is received by touch. Host plant selection 

241 
and orientation on leaf surface depend considerably on composition of the cuticular wax components. 

These components determine, for example, host plant selection by the aphid Acyrthosiphon pisum Harr., 

stimulate egg laying by the fly Pegomyiabetae Curt., and increase the number of feeding probes by the 

weevil Sitona lineatus L. (Klingauf et al. 1978). The cuticular wax composition also influences host 

plant selection by the aphid Tuberculoides annulatus Hart. (Kennedy 1986a ), but for this species 

microrelief of leaf surface is of greater importance. T. annulatus inhabits the rough leaves of Quercus 

robur, and does not like the smooth leaves of Q. ilex. Tarsi of the aphid Myzocallis schreberi, by 

contrast, can be easily fixed on smooth surfaces with the help of a drawing empodium (Kennedy 

1986b ). The tarsal morphology of the cicadid Empoasca fabae is adapted for fixation on smooth leaf 

surfaces, which is why this species avoids haired varieties of soya (Lee et al. 1986). Thus host plant 

preference is often determined by insect tarsus morphology. 

Hairs on the leaf surface inhibit insect movements and can prevent feeding or egg laying. 

Although female Diaphania nitidalis and D. hyalinata moths are not able to distinguish extracts from 

hairy and hairless leaves of the cucumber Cucumis sativus in experimental conditions, they lay more 

eggs on smooth leaves. It is thought that this preference is a function of tactile stimulation (Elsey and 

Wann 1982). 

The physiological condition of the host plant also affects insect development. Plant weakening 

is sometimes known to be accompanied by a decrease in its resistance to pests. Decrease in resistance 

is caused, in turn, both by reduction of allelochemicals and changes in acidity and osmotic pressure of 

cellular liquid toward promotion of insect development (Radkevich 1980). Baranchikov (1983) divides 

factors of plant resistance into two groups: those based on origin--passive and active factors--and those 

based on direction of effect--general and specific factors. The passive factors are characteristic for a 

plant independent of its relations with insects, and active factors come into play as a response to 

damage. General resistance depresses successful development of all herbivorous species, specific 

resistance that of unspecialized herbivores only. During leaf ontogeny, specific resistance factors are 

replaced by general ones, accounting for the different food values of young, mature, and old leaves for 

specialized and nonspecialized consumers. 

The specificity in food preference is a general adaptation of phytophagous insects to a 

heterogenous, "spotted" habitat formed by host plant parts. The first detailed analysis of parasite 

specificity was made by Dogel (1962). According to Dogel, specificity is a norm of parasite response 

to environmental conditions or a close connection between parasites and their hosts. Slepyan (1973) 

extended the concept of specificity. He classified specificity into three forms: hostal, topical, and 

ontogenetic. Hostal specifi~ty is identical to that defined by Dogel. Slepyan called the preference by 

parasites for a certain place on or in the host body topical specificity. It is of great importance for 

less mobile organisms with highly localized feeding, mining moth caterpillars, for example. According 

to Slepyan, ontogenetic specificity is the ability of parasites to develop in host organs of a certain age 

and offering certain morphological and physiological conditions. Since in the vigorous plant the 

individual age of each serial homological part, such as leaves on the shoot, is strongly connected with 

its place among other metameres, topical and ontogenetic specificity are identical in the context of our 

work. The influence of host tree age on insect mine distribution has not been investigated. 

The irregularity of mine distribution in some spring moth species is connected with the dates of 

leaf appearance. For example, female Eriocraniidae moths deposit their eggs in birch buds, and that is 

why the larval mines are usually located on the first or second leaf of a shoot. This phenomenon may 

be called false topical specificity. 

Thus heterophylly and the heterogeneity of leaf parts, together with the ability of phytophagous 

insects to discriminate almost all morphological and physiological characteristics of host plants, lead to 

the irregularity of insect mine distribution on leaf parts, on leaves of shoots, and on the types of 

shoots put forth by host trees. 

242 
The objective of this paper is to describe the mine distribution of 34 moth species belonging to the 

families Nepticulidae, Tischeriidae, Gracillariidae, and Coleophoridae on 22 host tree species. 

MATERIALS AND METHODS 

Material for this work was collected from 1986 to 1989 in Leningrad, Murmansk, Moscow, 

Voronezh, Kiev, the Kujbishev districts, the Krasnodar and Primorje areas, and Georgia. 

Mine distribution on the parts of a simple leaf was investigated according to the method elaborated 

by Shevtchenko (1958). The leaf was subdivided into strips of equal area perpendicular to the central leaf 

rib and in twice the number of strips parallel to this rib. The number of mines was calculated in every 

rectangle of this net; data for right and left leaf parts were compiled. Equal strip areas allow us to 

describe the empiric functions of mine distribution along both coordinate axes of the investigated 

two-dimensional space. The ratio between the mine number and the rectangle area can be used to 

represent the niche structure in volumetric diagrams (Fig. 1 ). The height of the columns is related to the 

number of investigated mines, but the ratio between heights is specific for every insect and its host plant. 

The simpler method is the calculation of mine number in leaf parts between the lateral ribs. It should be 

noted that diagrams of mine distribution along the central leaf rib are different for the two described 

methods. 

The leaves on annual shoots, the leaflets of the compound leaf, and the parts of the simple leaf 

were numbered from the base to the top of the organ. The mine distribution on the crown of a tree is 

described by their ecological density: the share of mining leaves in a probe. Mine distribution on the 

different leaf parts was compared by Chi-square and lambda methods and Kholmogorov-Smirnoff criteria 

(Sachs 1972). 

The niche overlap of coexisting species was calculated according to Slobodchikoff and Schultz 

(1980): 

1 II l 

u = 1 - - L L I PIJ - q#J I 

2 i=l J=l 

where p ij and q1j are the mine frequencies of coexisting species in the rectangle with i and j coordinates, 

and n and k are the number of vertical and horizontal strips of the sample leaf. Mine localization on 

compound leaves or annual shoots was described by one coordinate (the number of leaves or leaflets), and 

niche overlap was calculated by the modified formula: 

1 II 

u = 1 - - L I Pt - q, I 

2 i=l 

A degree of interaction between coexisting species was measured by D/W ratio, where D is the 

difference between the mean value of resource consumption and W is the mean standard deviation (Giller 

1984). The ratio D/W < I indicates the potentially strong competition between coexisting species. The 

ratio D/W > 3 indicates that the interaction is all but absent. The D/W criterion can be used for the 

dome-like function only. Calculating niche overlap for the border values of this criterion we found 

a > 0.70 indicates strong competition and a < 0.26 the absence of interaction. 

Non-mined leaves with identical numbers gathered from equal annual shoots at the same height and 

on the same side of a tree crown were used to investigate leaf venation. The leaves were treated for 

lighting by sulfuric acid and alkali and colored by gentian violet and saphranin (Isakov et al. 1984). 

Venation density of leaf parts was calculated by measuring the number of crossings of ribs per unit of leaf 

length with an ocular ruler. The lighting conditions of mined and nonmined leaves were measured by 

luxmeter. The results were analyzed using standard statistical methods. 

243 
Figure 1. The scheme of leaf subdivision of the strips of equal area and 

volumetric diagram of niche structure: Stigmella ultima Pupl. on Acer mono 

(Primorye Region). 

RESULTS 

Types of Mine Distribution on the Host Plant 

Leaf Parts and Leaflets 

The distribution of mines over leaf parts was analyzed for 34 lepidopterous species on 18 host 

plants. Types of mine distribution over both sectors of simple leaves and over leaflets are similar. They 

are described by the convex curve with one maximum on 2 to 5 sectors or leaflets (Fig. 2). 

1\vo-dimensional analysis shows the pattern of mine distribution over simple leaves to depend on both 

insect species and host plant species. Significant distinctions in mine distribution are typical both for 

different moth species inhabiting the same host plant (Fig. 3) and for the single insect species feeding on 

different types of leaves on the same host plant. For example, the distributional pattern of Lithocolletis 

issikii Kum. mines on the large stool shoot leaves of Tilia cordata differs from that on ordinary leaves: 

x'- = 18.19 and 17.85; the level of significance for both coordinate axes is 0.99 (Fig. 4). The mine 

distribution of Lithocol/etis sp. on brachyblast and auxyblast leaves of aspen Populus ttemula also differ 

significantly (Fig. 5). The distribution of Lithocolletis issildi Kum. mines along the midrib of the leaves of 

Tilia cordata from short and long shoots differ with the level of significance 0.999 (x2 = 24.32 and 29.89 

respectively), as do the leaves of different areas. 

244 
% % 

fD 

a b 

c: • 

Figure 2. The mine distribution among the leaf parts of simple leaf (a) and 

among the leaflets of compound leaf (b): a- Stigmella malella Stt. on Malus 

domestics (Krasnodar); b- St. sorbi Stt. on Sorbus aucuparia (Leningrad). 

% 

2D 

a 

Figure 3. The mine distribution of coexisting species on leaf parts: 

a- Stigmella sp. and b- Lithocolletis malella Gram., both on Mespilus 

germanica (Georgia). 

245 

b 
% 

3D 

20 

-10 

{ 2 J it 5 6 7 a { 2 3 5 6 

Figure 4. The mine distribution on leaf parts of two leaf types: 

0 f 

•2 

7 

Lithocolletis issikii Kum. on Tilia cordata (Kiev). 1- shoot leaves, and 

b 

2 - ordinary leaves; a - parallel to central vein and b - perpendicular to it. 

a b 

Figure 5. The mine distribution on leaf parts of leaves from two shoot types, 

Lithocolletis sp. on Populus tremula (Leningrad): a- auxyblasts; 

b - brachyblasts. 

Comparison of mine distribution in four populations of L. issikii Kum. (from Kiev, Kuibyshev, 

Voronezh, and Moscow) showed geographical variability of this feature (Fig. 6); it is probably 

dependent on morphological and biochemical differences in leaves of host plant populations. The 

distribution of Stigmella nylandriella Tengstr. mines on leaflets of a compound rowan tree leaf differ 

246 
% % 0 4 

• 2 

Q 3 

0 It 

20 20 

10 ID 

I 2 .3 't 5 6 7 a 7 

Figure 6. The mine distribution of leaf parts in various geographical. 

regions, Lithocolletis issikii Kum. on Tilia cordata: 1 -Voronezh district, 

b 

2 Moscow district, 3 - Kujbyshev, 4 - Kiev; a - parallel to central vein and 

b - perpendicular to it. 

significantly in Murrnansk and Leningrad (x2 = 16.67 and 16.05; level of significance 0.95). That may be 

explained by climatic particularities of these regions or by the differences between host plants (Sorbus 

aucuparia in Leningrad and S. gorodkovii in Murmansk). 

Annual Shoots 

Mine distribution over the leaves of annual shoots was investigated for 18 lepidopterous species on 

13 host plants. In most cases, this distribution is described by the convex unimodal curve or its segments 

(Fig. 7). The polymodal character of some empirical distributions may be explained by insufficient number 

of calculated mines. 

Some empirical curves may approximate power, normal, or Poisson function, but the change of 

curve with the leaf number increase on the shoot is specific for every species, which is why their 

typification is nearly impossible. The mean number of injured leaves (calculated as arithmetic mean of 

injured leaf numbers) is the only comparable parameter of distribution. In most cases, the mean value 

increases with leaf number on the annual shoot. But for three species--Stigmella sorbi Stt., Caloptilia 

syringella F., and Lithocolletis issikii Kum. first generation--the maximum is observed on the shoots of the 

middle length. 

The pattern of mine distribution on annual shoots is connected with the systematic positioning of 

phytophagous insect species. Accordingly, the nepticulid moths prefer first leaves of shoots (Fig. 7a), while 

the gracillariid moths choose leaves in the middle of shoots (Fig. 7b ). On the other hand, host plant 

species can also be a factor in the mine distribution. For example, in Murmansk Territory, over 

247 
o a 

~ f; 

0 c 

f-2 :J-'1 s-6 7-8 9-10 

Figure 7. The mine distribution among the leaves of annual shoots of 

b 

(a) Stigmella malella Stt. and (b) on Malus domestica (Krasnodar): a= shoots 

with 4 to 5 leaves, b = 6 to 7 leaves, and c = 8 to 9 leaves. Horizontal 

scale = the leaf number; N- number of investigated mines. 

90 percent of Stigmella sorbi Stt. mines can be found on the first or second leaf of mountain ash shoots, 

but on the second or third leaf of Cotoneaster shoots (Kozlov and Koricheva 1989). 

Significant distinctions in mine distribution were discovered between three populations of Caloptilia 

syringella F. on common lilac and two populations of Lithocolletis issikii Kum. on small-leaf linden on 

shoots with five or more metameres. 

In some cases, the location of mines is determined by sequence of leaf blossom. In Voronezh 

Territory, the seventh leaf on the shoot of small-leaf linden blossoms out after egg laying by females from 

the hibernated generation of Lithocolletis issikii Kum. and so is not damaged by caterpillars of the first 

generation. Maximums of curves for mine distribution of the second generation are shifted toward the top 

of long shoots. That is why the mine distribution on shoots with six to seven leaves differs considerably 

for the first and second moth generations. 

Comparison of mine distributions over leaf sectors on common beech Fagus silvatica on shoots of 

different length and over leaves of different numbers on shoots of equal length, which was carried out for 

Lithocolletis maestingella M tiler showed no significant distinction between them. Thus the distribution of 

mines on the leaf does not depend on leaf position on the shoot. For five species, we compared the 

frequency of mines on the shoots of different length with the frequency of occurrence of these shoots on 

the host plant. These frequencies differ significantly for Lithocolletis sp. on speckled alder, Lithocolletis 

maestingella M tiler on common beech, and Caloptilia syringella F. on common lilac, which indicates a 

distinct preference for shoots with a certain number of metameres. 

248 
Crown Layers 

Mine distribution over crown layers was studied for four lepidopterous species. Most Caloptilia 

syringella F. mines are concentrated on the Syringa vulgaris and S. josikae bushes in the lower and middle 

layers of the crown, at a height of 40 to 120 em above ground surface, where shoots with 3 to 5 pairs of 

leaves are predominant. The upper layer of the crown consists of longer shoots with 7 to 12 metameres, 

where mines seldom occur. 

The maximal ecological density of Lithocolletis blancardella F. and Stigmella malella Stt. mines on 

the apple has been recorded at a height of 1.5 m (the normal tree height is about 4.5 m). 

Ecological density of first-generation mines of L. maestingella M tiler on common beech trees, about 

25 to 30 m high, decreases in the upper layer of the crown. This may be explained by a temperature 

gradient (in the spring the ground warms up more rapidly than the air). Ecological density of the second 

generation increases up to 25 m, then falls abruptly, probably because of the wind, which can blow the 

female moths away. In this case, mine distribution over both leaf sectors and annual shoots is similar in 

the various crown layers. This fact allows us to consider topical specificity and vertical changes in 

ecological density to be independent parameters jointly determining the distributional pattern of mining 

moths over a tree. 

Factors Influencing Mine Distribution Over the Host Plants 

Unlike other phyllophagous insects, mining caterpillars have no opportunity for food choice. Even 

nepticulid caterpillars, which make long serpentine mines, occur mainly near the place of egg laying. So, 

in both Stigmella oxyacanthella Stt. on Crataegus caucasica and St. confusella Wood. on Betula pendula, 

there are no distinctions in distribution of mines or eggs over the leaf surface (.A = 0.40 and 0.98 

respectively). Thus preference of place for oviposition by the female coincides with the food preferendum 

of caterpillars. 

Significant differences between distribution of mines with dead and living caterpillars of L. issikii 

Kum. on leaves of small-leaf linden (x2 = 12.68, level of significance 0.95) indicate the importance of the 

choice of oviposition place by this species. The survival of caterpillars is likely to depend on mine location 

on a leaf. 

Caterpillar distribution on the host plant can also be influenced by abiotic factors, among which 

illumination particularly important. Females of Malacosoma califomicum pluviale Dyar are shown to 

prefer the sunny side of the tree (Moore et al. 1988), moths of Stigmella malella Stt. prefer the shady 

leaves (Chambon 1968). Caloptilia syringella F., which occurs in the lower layer of the shrub crown, is 

known to damage most heavily the common lilac growing in shadow (Lazareva et al. 1985). Comparison 

of lighting conditions of leaves with and without mines, as well as our experiments with moth females, 

showed that the lilac moth lays eggs on less illuminated leaves. 

Biotic factors influencing mine distribution are diverse: leaf structure, density of herbivorous insect 

populations, and interspecific competition, among others. 

Experimental study of the behavior of Stigmella malella Stt. females before egg laying (Chambon 

1968) showed the moths of this species to prefer the prominent relief of ribs (lower side of a leaf). The 

degree of vascular system development and the peculiarities of leaf venation are of great importance for 

mining caterpillars. The investigation of leaf venation carried out on different parts of the leaf for Tilia 

cordata., Mespilus germanica, Fagus sylvatica, and Carpinus betulus showed a negative correlation between 

mine number and rib density for four of the 11 species of mining moths inhabiting these plants (Fig. 8). 

The coefficient of this correlation is not high (r = -0.14 to -0.24), but it is statistically significant. 

249 
% 

2 

0 f 

e2 

5 

n 

5.2 

s.o 

it.8 

. 't.6 

it. If 

% 

3 

a. f 2 .3 

0 i 

•2 

5 

n 

b 

Figure 8. The connection between vein density and mine distribution among the 

leaf parts, Coleophora sp. on Carpinus betulus (Kiev): a= perpendicular to 

central vein and b = parallel to it; 1 the mine distribution (left scale, 

percent) and 2 = the vein density (right scale, the number of vein crosses 

with 1 mm scale). 

In one case (Coleophora sp. on Carpinus betulus, r = -0.12), the choice of place for mine was made not by 

the moth, but by the caterpillar. Last instar caterpillars of this species leave the mine, build the case, and 

move freely on a leaf surface. They bore a hole in the epidermis and feed on mesophyll tissues, forming a 

bilateral mine. A negative correlation between mine number and density of ribs has been found for 

Stigmella sp. on Fagus silvatica and St. microtheriella Stt. and St. carpinella Hein. on Carpinus betulus, 

taking into account only initial parts of serpentine mines (r is -0.2 and -0.16 respectively). If we consider 

all leaf parts with a mine, the correlation becomes insignificant. Obviously, for caterpillars of the genus 

Stigmella Schr., the low density of leaf venation is necessary at early stages of mine formation only, when 

larval mandibles cannot penetrate the hard cover of leaf veins. The important role of moth females in 

choice of place with low rib density is confirmed by their peculiar behavior (Strokov 1956) and by the 

presence of sensory elements on the end of their abdomen (Chambon 1968). 

The pattern of mine distribution may depend on population density of herbivorous insects. For 

example, if the ecological density of Stigmella nylandriella Tengstr. in Voronezh Territory is low (about 1 

mine per a compound leaf of mountain ash), the distribution of leaflet areas and mines differs significantly 

(A = 2.32); if insect density increases up to 18 mines per leaf, distribution of the two becomes equal (A = 

0.48) (Kozlov and Koricheva 1989). Analogous "substrata saturation" was described for the gall midge 

Miciola fagi Hart., inhabiting beech, when its ecological density was increasing (Dajoz 1981 ). 

If the ecological density of herbivorous insects is low, their food resources are practically unlimited. 

Therefore, in case of joint utilization by a few species, food preferendums may coincide. But many 

phytophages and miners in particular sometimes become enormously abundant, damaging up to 90 percent 

of leaves (Petrenko 1967, Tshagelishvili 1972). In that case, the degree of environmental resource 

saturation decreases and, according to the competitive exclusion principle, the coexistence of species is 

possible only if there are some ecological distinctions between them. Coexisting species of mining moths 

have a similar food source; thus repeated resource utilization is impossible if there are temporal confines 

250 
between coexisting species. In that case, evidently, those dimensions of the niche which are connected with 

heterogeneity of host plant, i.e. the site parameters, must play the main role. 

The study of mine distribution in seven moth complexes on the leaves of annual shoots and the 

, parts of leaves indicates some interaction between coexisting species. In Kiev Territory, six species 

inhabiting the european hornbeam, Carpinus betulus, have in most cases strong coincidence in one leaf 

dimension and considerable discrepancy in the other. Mine distribution of Paromix carpinella Frey and 

Coleophora sp. differs significantly in both dimensions from the many other species, and, conversely, 

distribution of mines Stigmella microtheriella Stt. and Lithocolletis quinnata Geoffroy show no distinctions 

in either dimension. The last pair of species, in addition to four other species inhabiting european 

hornbeam, have a coefficient of niche overlap of more than 0.7, which suggests strong competition. 

Distinctions in both dimensions of a leaf are significant for pairs of species coexisting on elm, common 

beech, small-leaf linden, and medlar; the coefficient of niche overlap for them is less than 0.7. 

For species of Stigmella centifoliella Z. and Tischeria angusticolella Zett. in Kiev Territory, there is 

no difference in mine distribution on leaflets of compound leaves (A = 0.86, 0.99, and 0.51 for leaves with 

3, 4, and 5 leaflets respectively); coefficients of niche overlap are more than 0.7 (a = 0.79, 0.84, and 0.75). 

Among three species inhabiting mountain ash, Sorbus aucuparia, mine distribution over leaflets of 

compound leaves differs significantly only in two species; the coefficient of niche overlap is more than 0.7. 

However, mine distribution of these species on annual shoots overlaps considerably less (a = 0.53- 0.65). 

Distinctions between Stigmella sorbi Stt. and St. nylandriella Tengstr. gradually increase with growth of leaf 

number on mountain ash shoots, reaching their maximum on shoots with 7 to 8 leaves. The most 

considerable distinction between Stigmella sorbi Stt. and Lithocolletis sorbi Frey was recorded on shoots 

with 3 to 4 and 7 to 8 leaves respectively. Thus niche overlap of these species is maintained at a minimal 

level on all shoot types. 

If we assume that mine distribution is controlled by interspecific competition, our data should 

satisfy several criteria (Brown and Davidson 1977, Addicott 1978). First, the potential competition 

between species should be factored into analysis of their niche structure. In our case, the coexistence of 

species under the large overlap of mine distribution functions on leaf parts of simple and compound leaves 

can be explained by divergence of these species along other dimensions of resources, such as mine 

distribution over the leaves of annual shoots in three moth species mining the mountain ash. Moreover, 

ecological density of the majority of studied species was rather low (about 1 mine per leaf) and 

preferendum coincidence may be explained by the excess of resources. However, the tendency of optimum 

to diverge at least along one dimension is observed in general. 

The second criterion is the utilization of mutual resources by the competitors. The method of 

material collection (at one time on one host plant) and the detection of mines of different moth species on 

a leaf show that this criterion is correct for mining caterpillars. 

Third, the behavior of a certain species in nature must verify intraspecific competition. Its presence 

in the case of mining larvae is proved by the fact that more uniform mine distribution over the leaf is 

observed by an increase in ecological density of the species (Kozlov and Koricheva 1989). The increase in 

Lithocolletis Hbn. ( = Cameraria Chapm.) mortality has been shown experimentally to depend on high 

caterpillar density (Bultman and Faeth 1986a ). 

These data confirm the importance of competition in the mining moth guild, albeit indirectly. They 

have prompted some authors to propose the alternative hypothesis on the mechanisms of species diversity 

regulation in folivorous insects (Lawton and Strong 1981 ). They suppose that the population density of 

herbivorous insects is usually lower than the quantity of resources allows and that intensification of 

competition during outbreaks cannot play the decisive role in formation of community structure. 

Individual ecological reactions--to climate, host plant phenology, biochemistry, and distribution--together 

with isolation, migration, and the influence of predator and parasite, are of principal importance. 

251 
According to this view, the coexistence of species became possible not as a result of the mutual 

adaptation of potential competitors, but owing to the initial differences in their ecology. 

However, there is direct evidence of interspecific competition in coexisting herbivorous insect 

species. For example, it has been shown for four aphid species that the growth rate of each is higher in 

the absence of competitors than in the presence of other species on the host plant (Addicott 1978). 

Besides, among folivorous insects the competition for food can be observed even at low ecological density, 

since plants, and in particular their vegetative organs, have low nutritional value and contain secondary 

metabolites. Such a situation might be typical when competitors are abundant. In nature one usually 

finds only a slight competition between a few species in the community. This can probably be explained by 

the fact that competition is too powerful a factor, one which during the evolution process either forces out 

one of the competing species or causes them to diverge into different niche dimensions. The study of 

Far-Eastern Lithocolletis issikii Kum., which suddenly appeared some years ago in the European part of the 

U.S.S.R., is of particular interest in this regard. 

Irregularity of distribution of mining caterpillars is based on differences in the structure of various 

leaves (or their parts) and their location on host plants; it can be regarded as a result of insect-plant 

coevolution. Mine distribution reflects the specific oviposition behavior of females, which discriminate 

different features of a host plant. One of the mechanisms regulating mining moth diversity is species 

competition. The presence of competition is confirmed by the above-mentioned tendency toward 

differentiation of ecological niches of potentially competing species. The role of different factors in the 

formation of associated mining moth structures is a question requiring further study. 

CONCLUSIONS 

Mine distribution over a simple leaf and over the leaflets of a compound leaf is irregular and 

specific for each moth and plant species. Mine distribution of a certain species can differ if the host 

plant's leaves are very heterogenous, as are the leaves of auxyblasts and brachyblasts, stoll shoots leaves, 

and ordinary leaves, and if the leaves are of different size and located on shoots of different length. 

For four moth species, the geographical variability of mine distribution on leaf parts and leaves of 

annual shoots is shown. In the majority of cases, the mine distribution on leaves of annual shoots can be 

described by a convex unimodal curve or its rising or descending part. Species of the family Nepticulidae 

prefer the basal leaves of a shoot independent of host plant species; the family Gracillariidae prefers leaves 

from the middle part of a shoot. The species of host plant can also be an influential factor in the 

distributional pattern of mines, however. 

The mine frequency of three among five studied moth species on shoots of different length does not 

coincide with the frequency of these shoots on host plants. We can conclude that females choose a certain 

shoot type. Ecological density of mines at a certain crown layer is determined by light conditions and 

possibly by different distribution modes of shoots in the crown. For 4 out of 11 studied species of mining 

moths, a significant negative correlation between mine number and vein density on leaf parts was 

discovered. This correlation can become insignificant with development of a mine. 

Significant distinctions in damage frequency of lilac leaves by Caloptilia syringe/fa F. mines were 

discovered in different light conditions. The moths of this species prefer shadowed leaves. Significant 

distinctions in mine distribution along at least one resource dimension were discovered for coexisting 

species. The irregularity of mine distribution on host plants results from active choice of the ovipositional 

place by moth females. This choice is influenced by both biotic factors, such as veins density, herbivorous 

insect population density, and interspecific competition, and abiotic factors, such as light conditions. 

252 
ACKNOWLEDGMENTS 

We are grateful to Drs. V. Kuznetzov (Zoological Institute, Leningrad), A. Sazonov (AU-Union 

Research Institute for Plant Protection, Leningrad), and A. Stekolnikov (Leningrad State University) for 

critical analysis of the manuscript, to Drs. A. Frolov, R. Noy, L Danilkina (Leningrad State 

University), and V. lsakov (Botanical Garden of the Latvijan Academy of Sciences, Riga) for help in 

leaf preparation. Dr. E. Zvereva (All-Union Research Institute for Plant Protection) provided 

invaluable assistance in manuscript editing and translation. 

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255 
ADELGID AND SCALE INSECT GUILDS 

ON HEMLOCK AND PINE 

MARK S. McCLURE 

Connecticut Agricultural Experiment Station 

Valley Laboratory, P.O. Box 248, 153 Cook Hill Road 

Windsor, cr 06095 U.S.A 

INTRODUCfiON 

Five piercing and sucking insects which were accidentally introduced from Asia during this 

century, together with one native species, have become very serious pests of two important forest tree 

species in the northeastern United States. Two armored scales, Fiorinia externa Ferris and Nuculaspis 

tsugae (Marlatt), and an adelgid, Adelges tsugae Annand, attack eastern hemlock, Tsuga canadensis 

Carriere (Fig. 1 ). A margarodid scale, Matsucoccus resinosae Bean and Godwin, and two adelgids, 

Pineus boerneri Annand and Pineus coloradensis (Gillette), attack red pine, Pinus resinosa Aiton (Fig. 2). 

In Japan, their homeland, F. externa and N. tsugae are common inhabitants of two native 

hemlocks, Tsuga diversifolia Masters and Tsuga sieboldii Carriere. However, these scales seldom attain 

injurious densities in Japan. Both scales were introduced accidentally into the vicinity of New York 

City about 80 years ago and have since become serious pests of T. canadensis in several northeastern 

states (Fig. 3). Both scales feed together on the needles of hemlock by sucking cell fluids from the 

mesophyll. In the United States their densities often increase rapidly to levels which cause needles to 

discolor and drop prematurely and branches to die. Many ornamental and forest trees have been killed 

in 10 or fewer years after infestation. 

Adelges tsugae is probably also native to Japan, where it is a harmless inhabitant of 

T. diversifolia and T. sieboldii. This adelgid was first noticed in North America 70 years ago on Tsuga 

heterophylla Sargent in British Columbia. It now occurs throughout much of that province and the 

northwestern United States, where its damage has been rare. In the eastern United States, A. tsugae 

was first reported 30 years ago on T. canadensis in Virginia. Since that time it has spread primarily 

northeastward and now occurs as far north as New England (Fig. 3) (McClure 1987a). Unlike the 

mesophyll-feeding scales, A. tsugae sucks sap from the phloem parenchyma of the young branches, 

causing rapid desiccation and drop of needles, dieback of main limbs, and death of the tree, usually 

within 2 years. 

Another Japanese species, M. resinosae, now considered to be the same species as 

M. matsumurae (Kuwana) (McClure 1983a), was first discovered in Connecticut in 1946 in a dying 

plantation of P. resinosa. Historical evidence suggests that this scale was introduced into the United 

States on exotic pines planted at the New York World's Fair in 1939 (McClure 1983a). This scale 

sucks sap from the phloem parenchyma of the 3-year-old wood, which causes desiccation and dieback 

of branches and tree death within 2 to 5 years. In China, where it was probably also introduced 

(McClure 1983a), M. resinosae has caused extensive injury to Pinus densiflora Siebold, P. thunbergiana 

Franco, and P. tabulaeformis Carriere. In Japan injury from this scale is rare and occurs only on 

cultivated trees (McClure 1983a). 

BARANCHIKOV, Y.N., MATfSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

256 
A 

B 

Figure 1. Guild species on Tsuga canadensis: nymphs and adults of the 

diaspidid scales, Nuculaspis tsugae (A) and Fiorinia externa (B), on the 

needles (lOX magnification); and ovipositing adults of the adelgid, Adelges 

tsugae (C), on the branches (3X magnification). 

The adelgid P. boemeri was probably introduced from Japan on the same pines that carried 

M. resinosae to North America (McClure 1982). This adelgid feeds primarily on the 3-year-old wood, 

where it sucks sap from the phloem parenchyma and causes the same type of damage as M. resinosae. 

257 
Unlike the scale, however, P. boerneri also feeds within the needle sheaths. Following their introduction 

50 years ago, both M. resinosae and P. boerneri expanded their ranges northward (Fig. 3). The adelgid 

has spread much more quickly than the scale because P. boerneri completes more generations each year 

and because the occurrence of its wind-dispersed nymphs coincides more closely with the prevalence of 

winds from the southwest (McClure 1989a ). 

The native adelgid, P. coloradensis, attacks only the exposed parts of the needles of its host, 

where it sucks sap from mesophyll cells. Until recently the impact of this adelgid on P. resinosa was 

inconsequential (McClure 1982). However, during the past few years, trees have become increasingly 

less resistant to P. coloradensis, possibly because of a host response to stressful environmental 

conditions (McClure 1989c). 

GUILD SPECIES INTERACTIONS WITH THEIR HOST PLANTS 

Host Responses to Herbivore Attack 

Adelgids and scales can induce a wide variety of defensive and pathological responses in the host 

plant, a discussion of which extends far beyond the scope of this report. Barbosa and Wagner (1989) 

devote an entire chapter to a discussion of the impact of piercing and sucking insects on trees and may 

be consulted for details. In general, adelgids and scales injure the host by removing sap and/or by 

injecting a toxic saliva during feeding. Effects on the host include reduced growth and vigor, physical 

destruction of host tissues, deformation of plant parts, alterations in host physiology and biochemistry, 

and increased susceptibility to destructive secondary agents such as unfavorable weather, disease, and 

other insects. Often the damage is insidious, the plant gradually losing vigor and only portions of it 

eventually dying. Populations of the introduced adelgids and scales, however, often multiply rapidly 

and kill their new host plants. 

The mechanism by which the insect guilds on hemlock and pine bring about the rapid decline of 

their host plants has not been investigated. However, in related species of adelgids and margarodid 

scales which also feed on the cortical parenchyma, saliva introduced into the plant during feeding 

triggers an imbalance in plant growth hormones (Puritch and Petty 1971). This causes structural 

modification of the xylem, restriction of water uptake by the sapwood, and rapid desiccation and death 

of the tree. 

Red Pine 

The impact of feeding by M. resinosae and P. boerneri on P. resinosa is similar to that reported 

for Matsucoccus josephi on Pinus halepensis and Pinus eldarica (Mendel and Liphschitz 1988) and for 

Adelges piceae on Abies balsamea (Hain 1988). Studies comparing the growth of infested and 

uninfested P. resinosa in the greenhouse and in a field plot revealed that relatively low densities of 

M. resinosae and P. boemeri reduced the biomass of new growth by 72 percent and of older (1- to 

3-year-old) growth by 53 percent. Branches became distorted and cracked and emitted copious 

quantities of resin from wounds in response to attack by these insects. The needle-feeding 

P. coloradensis caused a more insidious injury by reducing the photosynthetic capability of the tree. 

However, when infestations of this adelgid attain high density, as they have in recent years (McClure 

1989c), the loss of needles can be substantial and lethal to the host. 

The deleterious impact of A. tsugae on hemlock is sudden and usually lethal. Feeding by 

nymphs on the preferred youngest branches inhibits production of new growth from these branches 

during the following year. A single feeding nymph is sufficient to elicit this response in areas of the 

branch distal to the attack zone. Only 2 percent of the buds present per 0.5 m length of infested 

hemlock branch were viable the following year, and viable buds produced only 4.3 ± 0.5 mg of new 

258 
Figure 2. Guild species on Pinus resinosa: cysts (2nd instar nymphs) of the 

margarodid scale, Hatsucoccus resinosae (A) (12X magnification); adults of the 

adelgid, Pineus boerneri (B) (20X magnification), on the branches; and nymphs 

and adults of the adelgid, Pineus coloradensis (C) (2X reduction), on the 

needles. 

~9 
Figure 3. Current distributions (area below each line) of the introduced 

adelgids and scales on T. canadensis and P. resinosa in Connecticut (C), 

Massachusetts (M), and Rhode Island (RI). The species are A. tsugae (A.t.), 

F. externa {F.e.), and N. tsugae (N.t.) on hemlock, M. matsumurae (-

H. resinosae) {M.m.) and P. boerneri (P.b.) on pine. 

growth. Within trees this effect was quite localized; all of the buds produced on uninfested branches 

of infested trees were viable and produced 71.2 ± 6. 7 mg of new growth the following year. 

Eastern Hemlock 

The impact of the mesophyll-feeding scales on hemlock is much less severe than that caused by 

A. tsugae feeding on cortical parenchyma. The main impact of F. externa and N. tsugae is the 

reduction in energy reserves and photosynthetic capability of the host resulting from the premature loss 

of existing foliage and the retardation of new foliage production. Hemlocks infested with these scales 

for 5 years supported only one-third the total foliar biomass and produced only half as much new 

growth as their uninfested counterparts. Five to 10 successive years of this photosynthetic deficiency 

usually kill the tree. Feeding by these scales also reduced the nutritional quality (nitrogen 

concentration) of current and subsequently produced foliage (McClure 1980a). We shall see that 

nitrogen is important to the performance of this guild on hemlock and pine. 

260 
Herbivore Responses to Host Changes 

These species on hemlock and pine display strong preferences in their selection of colonization 

sites on the branches and needles. The preferences reflect physical and chemical attributes of these 

colonization sites. Hemlock and pine respond to attack by reducing the availability and suitability of 

these preferred colonization sites, which adversely affects the performance of these insects. For 

example, M. resinosae and P. boerneri preferentially colonize the 3-year-old pine branches where the 

fissured, flaky bark offers protection from inclement weather and natural enemies (McClure 1990). As 

densities of these insects increase, resinosis from wounds at the preferred feeding site engulfs and kills 

many of the older settled nymphs. It also forces the young mobile nymphs to colonize less suitable 

younger branches, where they subsequently incur significantly greater mortality from exposure to harsh 

weather conditions and from natural enemies (McClure 1977a, 1987b ). Similarly, the needle-feeding 

adelgid, P. coloradensis, shifts its colonization sites to the branches as pines deteriorate in response to 

attack. Nymphs feeding on the branches incur nearly twice as much mortality as those feeding on the 

needles (McClure 1984). 

One of the responses of hemlock to attack by these species is a significant reduction in the 

quantity of new growth produced. The two needle-feeding scales and the wood-feeding adelgid prefer 

to colonize the youngest growth (Table 1 ), where survival is significantly greater than on older growth 

(McClure 1980b) (Table 1 ). Therefore, as in the pine guild, the reduced availability of preferred 

colonization sites on hemlock following herbivore attack has a substantial deleterious impact on the 

performance of the hemlock guild species. 

Changes in the quality of feeding sites on hemlock and pine in response to herbivory also have 

profound effects. For example, life table data revealed that the single most important factor leading to 

the collapse of M. resinosae populations on P. resinosa was a change in the magnitude of overwintering 

mortality incurred by nymphs (McClure 1983b ). Drastic reductions in scale numbers in the winter 

more than offset population growth during the rest of the year and resulted in overall annual 

population decline. Steadily increasing overwintering mortality from year to year was due to a steadily 

decreasing developmental rate, which resulted from scale-induced reductions in the nutritional quality of 

feeding sites. The reduced developmental rate caused nymphs to overwinter at a younger age, when 

they were incapable of surviving even relatively mild winter conditions. 

Table 1. Percent of Fiorinia externa, Nuculaspis tsugae, and Adelges tsugae 

colonizing youngest and 1-year-old growth and percent survivorship 

of nymphs on that growth. For each parameter, means (+ 1 SD) in each 

row followed by different letters differ significantly (p < 0.05) by 

ANOVA. 

Colonists (%) Survival (%) 

Species Young 1-yr-old Young 1-yr-old 

F. externa 91.2 ± 17.5a 8.8 ± 5.7b 87.2 ± 2.5a 82.6 ± 0.9b 

N. tsugae 61.8 ± 13.8a 38.2 ± 9.2b 78.6 ± 4. 7a 72.0 ± 5.2b 

A. tsugae 83.4 ± 6.3a 16.6 ± 2.4b 54.2 ± 6.7a 15.4 ± 3.6b 

261 
The nutritional quality of food for piercing and sucking insects has often been linked to the 

quantity of organic nitrogen available to nymphs. Indeed extensive studies have demonstrated the 

importance of nitrogen to the performance of these species on pine and hemlock. For example, 

fertilization experiments revealed that nymphs of F. externa incurred 13 percent less mortality and each 

adult produced 45 percent more offspring on hemlocks whose foliar nitrogen concentrations had been 

elevated only 1 percent above the unfertilized controls (Table 2). The performance of A. tsugae was 

also enhanced by fertilization, as nymphs incurred 48 percent less mortality and each adult produced 

twice as many offspring on fertilized trees as on unfertilized ones (Table 2). 

Results of greenhouse and forest experiments have shown that the nutritional quality of hemlock 

typically declines as the host responds to attack by these insects (McClure 1980a). Concentrations of 

foliar nitrogen were reduced by an average of 18 percent after only 7 weeks of feeding by F. extema; 

concentrations of nitrogen in young needles were nearly three times higher on uninfested hemlocks 

than on those which had been infested previously (McClure 1980a). Clearly, deterioration in both the 

quantity and quality of colonization sites as hemlock and pine respond to attack have a significant 

negative impact on the performance of these species. 

SPECIES INTERACTIONS WITHIN THE GUILD 

Density-Dependent Feedback 

There is substantial evidence from both pine and hemlock that dense adelgid and scale 

populations significantly limit the success of individuals of subsequent generations. Because these 

species rapidly attain high population levels, density-dependent negative feedback is a common feature 

of their population dynamics. We have seen that density-dependent reduction in nymphal 

developmental rate is the most important factor in the population dynamics of M. resinosae. Other 

fitness parameters of this scale are also affected by density-dependent feedback. The relationship 

between scale density and scale performance was examined over a 6-year period from population 

increase to decline in a plantation of P. resinosa in Connecticut (McClure 1983b ). Initially when scale 

density was low and injury to trees was minor, survival and developmental rate of nymphs and 

fecundity of adults were not correlated with density. However, as density increased and pines became 

significantly injured, each of these fitness parameters was negatively correlated with scale density. Even 

Table 2. Effect of fertilization on foliar nitrogen concentration and 

subsequent survival and fecundity of Fiorinia externa and Adelges 

tsugae. Numbers are means (± 1 SD).a 

Treatment 

Nitrogen 

in needles 

(% dry wt) 

Fertilized 5.6 ± 0.4 

Unfertilized 4.3 ± 0.4 

F. externa 

Survival Eggs per 

of nymphs female 

(%) (number) 

81.5 ± 4.6 

68.5 ± 7.9 

13.3 ± 2.1 

9.3 ± 1.9 

A. tsugae 

Survival Eggs per 

of nymphs female 

(%) (number) 

79.8 ± 16.7 

31.3 ± 8.6 

98.2 ± 14.3 

49.8 ± 11.5 

•Differences in fitness parameters between fertilized and unfertilized trees 

were all significant (p < 0.005) by ANOVA. 

262 
though scale density decreased sharply after the fourth year, scale performance continued to decline, 

indicating that the deterioration of P. resinosa as a host was progressive and irreversible. 

Similar density·dependent feedback has been observed among the other species of this guild on 

pine. Survival, developmental rate, and fecundity of P. boerneri and P. coloradensis were strongly 

negatively associated with their population densities during a 5-year period in forests throughout New 

England (McClure 1984, 1989a, 1990). However, as with M. resinosae, the performance of these 

adelgids continued to decline even after their densities fell in response to host deterioration. 

There is also substantial evidence for density-dependent feedback in the hemlock guild species. 

On heavily infested hemlocks, mortality of F. externa nymphs was four times greater, several more days 

were required to complete nymphal development, and up to 30 percent fewer eggs were produced per 

adult than on sparsely infested trees (McClure 1979). Further indication that density adversely affects 

hemlock scale reproductive rates was seen when scale populations rapidly resurged following pesticide 

spraying (McClure 1977b). Scales that survived on sprayed trees had significantly higher fecundity than 

did those on controls, probably because of improved host quality following reduced herbivore pressure. 

Studies in several hemlock forests in Connecticut have revealed that the performance of 

A. tsugae is also adversely affected by density-dependent feedback. The presence of this adelgid, even 

in low densities, inhibits production of new growth, which in tum causes high nymphal mortality in 

subsequent generations. Density also has a profound impact on the performance of the current 

generation of A. tsugae. Mortality of nymphs was 15 percent higher, and adults produced only 25 

percent as many eggs on heavily infested hemlocks as on sparsely infested ones (Table 3). 

Even more significant to the population dynamics of this adelgid, however, was the impact of 

density on the production of sexuparae, the winged stage which migrates to spruce. The life cycle of 

A. tsugae includes a wingless generation which remains on hemlock and a winged generation which 

must feed on and complete its development on certain Picea spp. (McClure 1989b ). Hemlock and all 

of the native and more prevalent exotic Picea spp. which occur in the northeastern United States are 

unsuitable hosts for the sexuparae of A. tsugae (McClure 1987a). Therefore, presumably, that portion 

of the adelgid population which develops into winged sexuparae each summer dies. As adelgid 

densities on hemlock increased, an increasing proportion of the nymphs developing in· summer became 

winged sexuparae. For example, on the sparsely infested trees, only about 14 percent of the population 

became sexuparae, whereas on the heavily infested trees, nearly 90 percent of the population became 

sexuparae and dispersed from hemlock in an unsuccessful attempt to locate a suitable Picea host 

(Table 3). Clearly, this density-dependent feedback mechanism has a significant impact on the 

dynamics of A. tsugae populations on hemlock. 

Interspecific Competition and Competitive Exclusion 

All the exotic species discussed herein invaded New England from the southwest and now, 

therefore, have similar geographic distributions (Fig. 3). As a result, two or more species often occur 

on the same trees. However, extensive studies of both hemlock and pine have revealed that species 

compete intensely and that coexistence is transient. Interspecific competition leading to competitive 

exclusion is common in both guilds. 

P. coloradensis versus P. boemeri 

Studies in the greenhouse and in four cohabited pine stands in Connecticut revealed that 

P. boerneri established and maintained numerical dominance over P. coloradensis (McClure 1984). 

Decreasing density of P. coloradensis in mixed infestations has been caused by a combination of greater 

mortality on needles and greater colonization of bark, where chances for survival are poor. Population 

trends of these adelgids during a 5·year period in 15 pine forests in southern New England suggest 

263 
Table 3. Relationship between density of Adelges tsugae nymphs feeding on 

young hemlock branches and their subsequent survival, fecundity, and 

development. Means (± 1 SD) in each column followed by different 

letters differ significantly (p < 0.001) by ANOVA. 

Number of 

adelgids per 5 em 

33.6 ± 3.9a 

62.9 ± 7.7b 

Mortality of 

nymphs (%) 

19.7 ± 6.0a 

34.3 ± 8.8b 

Number of eggs 

per female 

105.2 ± 21.0a 

28.1 ± 11.0b 

Sexuparae 

(%) 

14.3 ± 1.6a 

88.4 ± 9.2b 

that P. boemeri has displaced P. coloradensis in all three previously cohabited pine stands and in 7 of 

12 others where P. coloradensis initially had occurred alone and where P. boerneri invaded subsequently 

(McClure 1989c). In four of the five remaining stands in the latter category, P. coloradensis had been 

reduced to very low density. These results reaffirm the superior competitive ability of P. boemeri 

demonstrated in greenhouse experiments. 

P. boemeri versus M. resinosae 

Later experiments in the field revealed that the performance of P. boemeri feeding both on 

branches and on needles of P. resinosa was significantly reduced by the presence of M. resinosae, which 

fed only on branches (McClure 1990). The presence of P. boerneri had no significant reciprocal effect 

on the fitness of M. resinosae. Interspecific competition was a significant limiting factor for P. boemeri 

even though it fed on needles and M. resinosae did not. Population trends of these insects during a 

7 -year period in six cohabited pine stands substantiated the competitive superiority of M. resinosae 

(McClure 1990). The six stands which had been infested only with P. boemeri in 1979 were invaded by 

M. matsumurae between 1981 and 1983. In each of these stands the abundance of P. boemeri on 

needles and on bark declined sharply following invasion by M. resinosae (Fig. 4 ). In three of these 

stands (Haddam, Middletown, and Old Lyme), P. boemeri was excluded by its competitor within 3 years 

(Fig. 4). 

The earlier studies revealed that P. boemeri quickly excluded the ubiquitous native adelgid, 

P. coloradensis, from cohabited pine stands (McClure 1989c). Results of the later study indicated that 

M. resinosae in tum quickly displaced P. boemeri (McClure 1990). Unfortunately, competition among 

these species and the resulting sequential pattern of species displacement were of no obvious advantage 

to the besieged host, because even though total herbivore population density declined sharply in all 

pine stands (Fig. 4), the level of host damage sustained prior to that time was severe and often lethal 

(McClure 1990). 

N. tsugae versus F. externa 

Studies in the greenhouse and in hemlock forests in Connecticut established that F. extema and 

N. tsugae compete for food and space and that F. extema is the superior competitor (McClure 1980b, 

1983c). Comparison of mortality data from solitary and coexisting populations of these scales revealed 

that F. extema had a greater adverse effect on the survival of its competitor than N. tsugae had on 

itself, while N. tsugae had a less significant effect on F. externa survival than F. externa had on itself. 

This superior competitive ability of F. externa resulted from the nutritional advantage gained by 

colonization 2 to 4 weeks earlier than its competitor, when foliar nitrogen and water are more 

concentrated. Early feeding by F. externa not only reduced the amount of foliar nitrogen by the time 

264 
U) 

w 

..J 

c 

w 

w 

z 

............ 

U) 

w 

~ 

< 

..J 

LL. 

0 

0 

,.. 

a: 

w 

a.. 

a: 

w 

m 

~ 

~ 

z 

----~'as '79 -----• 'as '79 -----•'as 

Figure 4. Mean number of adelgids and scales on 100 needles and beneath 100 

bark flakes of P. resinosa in six cohabited stands in Connecticut from 1979 

through 1985. Within each bar are the proportions of the total insects that 

were Pineus boerneri (shaded area) and Hatsucoccus resinosae (unshaded area). 

Stars indicate the first year during which the crowns of all trees were at 

least 50 percent visibly damaged. Arrows denote the year during which 

H. resinosae first invaded the stand. Letters designate stands in the towns 

of Litchfield (L), Lyme (LY), Waterford (W), Haddam (H), Middletown (M), and 

Old Lyme (0). 

that N. tsugae colonized the needles, but also forced N. tsugae to colonize less nutritious older growth 

where scale success was significantly reduced (McClure 1980b ). 

Because of its competitive superiority, F. externa quickly excluded N. tsugae from mixed 

infestations in a field plot and in 20 hemlock forests in Connecticut (McClure 1980b ). In 12 forests in 

which F. extema outnumbered its competitor in the initial census, N. tsugae was eliminated after only 

3 years. However, even in eight forests in which densities of N. tsugae were initially sevenfold higher 

than those of F. extema, N. tsugae was eliminated after only 4 years (McClure 1980b). Similar results 

were obtained in the field plot experiment, wherein the relative abundance of N. tsugae on cohabited 

265 
trees was reduced from 66.9 percent of the total scales present to less than 1 percent in 4 years. The 

host-finding behavior of a parasitoid common to both scales also contributed to the rapid decline of 

N. tsugae populations (McClure 1980b ). 

A. tsugae versus Needle Scales 

During the past 4 years, A. tsugae has invaded many hemlock stands previously inhabited by one 

or both hemlock scales in southern New England (Fig. 3). The rapid desiccation and premature drop 

of hemlock foliage in response to attack by this adelgid have had an obvious impact on the 

needle-feeding scales. The immobile stages of these scales, which are firmly attached to the needles for 

11 months during the year, are immediately lost to the population when needles drop prematurely. 

The less obvious species interactions that occur prior to needle drop are currently being investigated. 

However, as in the pine guild, the level of herbivory and host deterioration needed to bring about a 

significant reduction in the abundance of hemlock guild species is severe and often lethal. 

Consequently, the intense competitive interactions among the guild species have been of no benefit to 

hemlock as these insects have expanded their distributions northward. 

CONCLUSIONS 

Factors Regulating Endemic Populations 

Studies on the population dynamics of the adelgids and scales of hemlock and pine in Asia 

revealed tJtat in native habitats these species were usually maintained at innocuous densities by the 

combined influence of host resistance and natural enemies. Experiments were conducted in Japan in 

pure and hybrid stands of Pinus species of the subsection Sylvestres (the group to which all known 

host species of M. resinosae belong) to determine their relative susceptibility to this scale. Survivorship 

of scale nymphs and fecundity of adults were significantly lower on the two native Japanese pines, 

P. densijlora and P. thunbergiana, and their interspecific hybrid than on several pure and hybrid pines of 

related exotic species (McClure 1985a). Maternal parents of Japanese species did not confer resistance 

upon the F1 progeny that resulted from hybrid crosses with susceptible exotic species. Overall trends 

in scale survivorship in 10 pure and hybrid stands indicated a chemical basis for host resistance. 

However, interspecific variation in bark texture and significant differences in survivorship of nymphs in 

exposed and protected sites on bark indicated a physical basis for host resistance as well (McClure 

1985a). · 

Life table data gathered from 30 ornamental and forest pine stands in Japan revealed that 

predators also have an important role in the regulation of endemic scale populations (McClure 1986a). 

The coccinellid beetle, Harmonia axyridis Pallas, native to Japan, comprised 84 percent of the total 

number (n = 3,071) of predators captured. It killed 97 percent of the scales in one heavily infested 

pine stand in less than 4 weeks. When realistic densities of beetles were caged on infested pines, 

81 percent of the small, inconspicuous life stages of the scale and 98 percent of the larger, more 

conspicuous life stages were consumed. This resulted in a 67 -fold decrease in scale population growth 

compared with control cages containing no beetles (McClure 1986a ). 

Other studies in Japan revealed that host resistance and natural enemies were important 

regulatory factors for populations of the scale and adelgid species on hemlock as well. Samples taken 

from 13 natural and cultivated stands of T. diversifolia and T. sieboldii throughout Honshu revealed that 

densities of F. externa and N. tsugae were always innocuous and low relative to those on T. canadensis 

in North America (McClure 1986b ). Density, survivorship, and fecundity of both scale species were 

significantly higher on hemlocks planted outside their natural range in Japan than on naturally 

occurring montane trees, and significantly higher on Tsuga species exotic to Japan than on Japanese 

hemlocks (McClure 1986b). I infer from these and other results (McClure 1983d) that trees growing 

266 
outside their natural habitats are less resistant to insect herbivores, presumably due to stress from less 

adequate growing conditions and fewer natural enemies (more enemy-free space). 

Data from a field plot study and life table data gathered from 13 sites in Japan revealed that 

endemic populations of these scales have the potential to attain densities injurious to host hemlocks, 

especially trees in cultivation (McClure 1986b). However, this seldom occurs because of the 

hymenopteran parasitoid, Aspidiotiphagus citrinus Craw, which regularly killed more than 90 percent of 

both scale species (McClure 1986b ). 

Implications for Developing Management Strategies 

Maintenance of Host Plant Vigor and Resistance 

Clearly, the Asian species of hemlock and pine are inherently much more resistant to their 

native adelgids and scales than are their North American counterparts. What little resistance there 

may be among individual North American hemlocks and pines to attack by these introduced species has 

been impossible to detect because of the speed with which these insects attain high and lethal 

population densities. This situation, combined with the relatively high degree of genetic homogeneity 

known for P. resinosa, has inhibited development of genetically resistant lines which could be used in a 

pest management program. Results from my studies of two sap-feeding guilds support the hypothesis 

that trees under stress are less resistant to attack by endemic species than are healthy trees (McClure 

1983d, 1985a, 1985b, 1986b). Further studies are needed to verify that hemlocks and pines growing in 

cultivation or outside their natural range are stressed and are less resistant to herbivores than are 

naturally growing trees. Nevertheless, the rapid rates of increase of endemic species on cultivated trees 

emphasize the need to maintain host vigor as well as the danger of planting tree species outside their 

natural ranges. 

A lengthy discussion of the various silvicultural practices that can be used to maintain host vigor 

and resistance to herbivores is beyond the scope of this report. However, one practice for improving 

the vigor of plants, fertilization, warrants some consideration in view of my studies. We have seen in 

Table 2 that adelgids and scales on hemlock were favored by increases in the soluble nitrogen 

component of their food; their performance on fertilized trees was significantly higher than it was on 

unfertilized trees. Therefore tree "feeding" as a management tool for piercing and sucking insects 

should be used with discretion. 

Establishment and Preservation of Natural Enemies 

Earlier I reported that natural enemies also play an important regulatory role in endemic 

populations of guild species on hemlock and pine in Asia. A popular approach for controlling 

injurious populations of introduced species has been the introduction and establishment of natural 

enemies from the homeland of the pest. Examples of successful biological control, however, are 

relatively scarce despite great efforts over many years. Such has been the case for biological control 

efforts in Connecticut against M. resinosae using its effective native predator, H. axyridis, and against 

F. externa and N. tsugae using their effective native parasitoid, A. citrinus. The reasons for the failure 

of these biological control agents are quite different and reflect the complexity of coevolved 

host-herbivore-natural enemy interrelationships. 

The apparent failure of H axyridis to establish itself as an effective predator of M. resinosae in 

Connecticut has been attributed to its limited ability to exploit all life stages of the scale and to 

overwinter (McClure 1987b ). Cage experiments in Connecticut revealed that H axyridis can 

significantly reduce the abundance of M. resinosae only when the conspicuous life stages (eggs, cysts, 

and adults) are present. This beetle is ineffective during those other times of the year when scales are 

first instar nymphs concealed in the cracks and crevices of the bark. In Japan, H. axyridis is an 

267 
effective predator throughout the year because the relatively untextured bark of Japanese pine species 

does not afford as much protection for first instar nymphs as does the textured bark of P. resinosa 

(McClure 1985a, 1986a, 1987b). Results of two overwintering experiments in Connecticut indicated 

that the ability of H. axyridis to survive winter conditions in its new environment was also limited 

(McClure 1987b ). Less than 10 percent of the adult beetles (n = 762) placed in cages in the field 

survived from November through March, a period during which weather conditions were normal for 

Connecticut. 

Even more frustrating has been the failure of A. citrinus to control populations of the exotic 

hemlock scales in Connecticut, where this parasitoid is already widely established. Throughout Japan 

the seasonal occurrence of adult parasitoids and vulnerable stages of both scale species were 

synchronous, resulting in high parasitism rates and population regulation (McClure 1986b). In contrast, 

Connecticut populations of A. citrinus are asynchronous with their scale hosts because of phenological 

differences. This results in inconsistent parasitism rates and unregulated populations of these exotic 

scales which injure and kill their new host (McClure 1986b ). 

Outlook 

Managing endemic populations of guild species on hemlock and pine may simply involve 

adherence to silvicultural practices that maintain tree vigor and preserve the natural enemy community. 

The management of introduced populations of these insects will be a much more difficult task. Even 

vigorous stands of hemlock and pine have shown no resistance to the build-up of injurious adelgid and 

scale populations, and important natural enemies in Asia have been ineffective in North America. 

Chemical control of some of these guild species has been achieved on trees where complete coverage 

of the foliage with pesticide was obtained. However, it has been virtually impossible to obtain 

complete coverage in forests, and incomplete pesticide spraying has resulted in the rapid resurgence of 

populations (McClure 1977b ). The best and perhaps the only permanent solution for the control of 

the introduced species on T. canadensis and P. resinosa may be the identification or development 

through genetic manipulation of effective natural enemies and resistant hosts. Until more effective and 

persistent natural enemies are found, we must strive to maintain vigorous stands of hemlock and pine 

and to use pesticides only when needed, and then as prudently as possible to minimize their deleterious 

impact on existing natural enemies. 

SUMMARY 

An herbivore guild comprised of endemic species is often the product of a long coevolutionary 

struggle between herbivores and their host plant. Examples of neatly structured coevolved guilds 

permeate the literature and are highlighted elsewhere in these proceedings. Far less structured and less 

stable are guilds comprised of introduced species in which herbivores have had little or no 

coevolutionary history with their new host plants. In such guilds, resource partitioning, species packing, 

and other such intimate relationships that often characterize guilds of endemic species are seldom 

apparent. Instead, with little resistance from the new host plant, and in the absence of native natural 

enemies, introduced herbivores often multiply rapidly to a level at which deteriorating resources limit 

further population growth. Therefore hostile competitive interactions often characterize these guilds, 

and the success of each member species is usually measured by its relative ability to cope with the 

harmful effects of herbivory on the food supply. My studies revealed that the herbivore guilds 

comprised of Asian species of adelgids and scales on North American species of hemlock and pine are 

indeed highly interactive, unstable, and destructive to their host plants. Finally, I discuss the 

interactions between the guild species and between them and their hosts, and the ramifications for 

population dynamics and management of these insects. 

268 
LITERATURE CITED 

BARBOSA, P. and WAGNER, M.R. 1989. Introduction to Forest and Shade Tree Insects. Academic 

Press, New York. 639 p. 

HAIN, F.P. 1988. The balsam woolly adelgid in North America. In Berryman, A.A., ed. Dynamics of 

Forest Insect Populations: Patterns, Causes, Implications. Plenum, New York. 

McCLURE, M.S. 1977a. Population dynamics of the red pine scale, Matsucoccus resinosae (Homoptera: 

Margarodidae ): the influence of resinosis. Environ. Entomol. 6: 789-795. 

McCLURE, M.S. 1977b. Resurgence of the scale, Fiorinia extema (Homoptera: Diaspididae), on 

hemlock following insecticide application. Environ. Entomol. 6: 480-484. 

McCLURE, M.S. 1979. Self-regulation in populations of the elongate hemlock scale, Fiorinia extema 

(Homoptera: Diaspididae ). Oecologia 39: 25-36. 

McCLURE, M.S. 1980a. Foliar nitrogen: a basis for host suitability for elongate hemlock scale, Fiorinia 

externa (Homoptera: Diaspididae). Ecology 61: 72-79. 

McCLURE, M.S. 1980b. Competition between exotic species: scale insects on hemlock. Ecology 

61: 1391-1401. 

McCLURE, M.S. 1982. Distribution and damage of two Pineus species (Homoptera: Adelgidae) on red 

pine in New England. Ann. Entomol. Soc. Am. 75: 150-157. 

McCLURE, M.S. 1983a. Temperature and host availability affect the distribution of Matsucoccus 

matsumurae (Kuwana) (Homoptera: Margarodidae) in Asia and North America. Ann. Entomol. 

Soc. Am. 76: 761-765. 

McCLURE, M.S. 1983b. Population dynamics of a pernicious parasite: density-dependent vitality of red 

pine scale. Ecology 64: 710-718. 

McCLURE, M.S. 1983c. Competition between herbivores and increased resource heterogeneity, 

p. 125-153. In Denno, R.F. and McClure, M.S., eds. Variable Plants and Herbivores in Natural 

and Managed Systems. Academic Press, New York. 

McCLURE, M.S. 1983d. Reproduction and adaptation of exotic hemlock scales (Homoptera: 

Diaspididae) on their new and native hosts. Environ. Entomol. 12: 811-815. 

McCLURE, M.S. 1984. Influence of cohabitation and resinosis on site selection and survival of Pineus 

boemeri Annand and P. coloradensis (Gillette) (Homoptera: Adelgidae) on red pine. Environ. 

Entomol. 13: 657-663. 

McCLURE, M.S. 1985a. Susceptibility of pure and hybrid stands of Pinus to attack by Matsucoccus 

matsumurae in Japan (Homoptera: Coccoidea: Margarodidae). Environ. Entomol. 14: 535-538. 

McCLURE, M.S. 1985b. Patterns of abundance, survivorship, and fecundity of Nuculaspis tsugae 

(Homoptera: Diaspididae) on Tsuga species in Japan in relation to elevation. Environ. Entomol. 

14: 413-415. 

McCLURE, M.S. 1986a. Role of predators in regulation of endemic populations of Matsucoccus 

matsumurae (Homoptera: Margarodidae) in Japan. Environ. En to mol. 15: 976-983. 

269 
McCLURE, M.S. 1986b. Population dynamics of Japanese hemlock scales: a comparison of endemic 

and exotic communities. Ecology 67: 1411-1421. 

McCLURE, M.S. 1987a. Biology and control of hemlock woolly adelgid. Bull. Conn. Agric. Exp. Stn. 

851. 9 p. 

McCLURE, M.S. 1987b. Potential of the Asian predator, Harmonia axyridis Pallas (Coleoptera: 

Coccinellidae) to control Matsucoccus resinosae Bean and Godwin (Homoptera: Margarodidae) in 

the United States. Environ. Entomol. 16: 224-230. 

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McCLURE, M.S. 1989b. Evidence of a polymorphic life cycle in the hemlock woolly adelgid, Adelges 

tsugae Annand (Homoptera: Adelgidae ). Ann. Entomol. Soc. Am. 82: 50-54. 

McCLURE, M.S. 1989c. Biology, population trends, and damage of Pineus boerneri and P. coloradensis 

(Homoptera: Adelgidae) on red pine. Environ. Entomol. 18: 1066-1073. 

McCLURE, M.S. 1990. Cohabitation and host species effects on the population growth of Matsucoccus 

resinosae (Homoptera: Margarodidae) and Pineus boerneri (Homoptera: Adelgidae) on red pine. 

Environ. Entomol. 19: 672-676. 

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drying in Pinus halepensis and P. eldarica infested with Matsucoccus josephi. J. Exp. Bot. 

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270 
ADELGID HOST INTERACTIONS 

WITH SPECIAL REFERENCE TO THE 

BALSAM WOOLLY ADELGID IN NORTH AMERICA 

F.P. HAIN1 and R.G. HOLLINGSWORTH,1 

F.H. ARTHUR,2 

F. SANCHEZ,3 

and R.K. ROSS4 

1Department of Entomology 

North Carolina State University 

Raleigh, NC 27695 U.S.A 

2USDA Stored Products Insects R & D Lab 

Savannah, GA 31403 U.S.A 

3Department of Chemistry 

North Carolina State University 

Raleigh, NC 27695 U.S.A 

4Department of Genetics 

North Carolina State University 

Raleigh, NC 27695 U.S.A 

INTRODUCTION 

The objectives of this paper are: 1) to provide a general overview of adelgid biology and the 

various host relationships; 2) to review the current knowledge of the interactions of the balsam woolly 

adelgid, Adelges piceae (an introduced pest), and its North American hosts; 3) to report on the most 

recent research involving the interactions of this adelgid with Fraser fir, Abies fraseri, in the southern 

Appalachians; and 4) to provide a synthesis of the above in the form of an hypothesis regarding host 

tolerance for the balsam woolly adelgid. 

Adelgids are conifer-feeding insects in the super-family Aphidoidea of the order Homoptera. 

They are frequently referred to as aphids and have similar features such as a soft body and 

membranous wings. Both feed on plant sap. However adelgids are placed in a separate family, 

Adelgidae, because they differ from true aphids in having short antennal segments, a reduced wing 

venation, glandular body surface, no siphunculi, and because all the female forms are oviparous (Carter 

1971). 

The life cycles of species within the Adelgidae is either holocyclic, requiring a primary and 

secondary host, or anholocyclic, occurring only on one host. In the holocyclic life cycle the primary 

host is always a spruce (Picea) and the secondary host is a conifer of another genus such as fir (Abies), 

larch (Larix), pine (Pinus), Douglas-fir (Pseudotsuga), or hemlock (Tsuga). 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

271 
The holocyclic life cycle (e.g. Adelges laricis), as described by Carter (1971 ), is shown in Fig. 1. 

On the primary host, eggs are laid by a fertilized female (apterous sexuales). The egg hatches· into a 

fundatrix nymph that settles on the current year's shoot. After overwintering, feeding activity is closely 

synchronized with the flow of sap in the spring. The mature fundatrix females lay a large cluster of 

parthenogenetic eggs which hatch into gallicolae nymphs. As the nymphs feed on the sap of the young 

tissue the characteristic adelgid gall forms. During the summer the deformed needle bases which form 

most of the gall become separated, and the winged gallicola is released. Throughout the summer the 

gallicolae migrate to the secondary host (Larix in the case of A. laricis) where they settle on the 

needles and lay eggs. 

The parthenogenetic eggs of the gallicolae give rise to sistens and the first generation on the 

secondary host begins (Fig. 1 ). After overwintering as first or second ins tar sis tens, the sis tens mature 

in the spring and lay large clusters of eggs which hatch into progrediens nymphs. Two morphs of the 

progrediens nymph develop simultaneously into apterous oviparae and alate sexuparae. The latter 

migrate back to the new needles of spruce and lay eggs which hatch as males and females of the 

sexuales generation, and the entire life cycle is completed. The apterous progrediens may produce 

additional generations of progrediens or sistens during the summer. They overwinter as sistens and 

give rise to sexuales and progrediens the following spring. 

Anholocyclic adelgids do not have all the morphs in Fig. 1 and reproduction is by 

parthenogenesis exclusively. The life cycle may be confined to any one of the conifer genera. Carter 

(1971) described four types of anholocyclic adelgids. Two types are on spruce: one has gall-forming 

morphs that have the appearance of the fundatrices and gallicolae (e.g. Adelges abietis), the other type 

has only apterous forms and no galls are formed (e.g. Pineus pineoides). The other two types occur on 

the secondary host and produce sistens and progrediens; one type may produce sexuparae that are 

incapable of producing males (e.g. P. pini), the other type does not produce sexuparae although alates 

are produced which give rise to sistens (e.g. A. piceae). 

The focus of this paper, Adelges piceae, the balsam woolly adelgid, infests Abies species and is 

believed to be native to the silver fir, A. alba, forests of central Europe. The adelgid was introduced 

into North America around 1900. European firs are not seriously affected by this insect, but North 

American firs frequently experience either crown dieback or tree death or both. Adelgid-caused 

damage has been extensive and, at times, intense. 

Europeans place the true fir-infesting adelgids in the genus Dreyfusia (Borner 1908). The British 

and North Americans follow a classification that places all the sub-family Adelginae into two genera, 

Pineus and Adelges, based on the number of abdominal spiracles (Annand 1928, Carter 1971). This 

latter classification is used here. Three subspecies of A. piceae have been identified on the basis of 

morphometric analysis (Foottit and Mackauer 1980, 1983): A. piceae piceae, Pacific Northwest, British 

Columbia, and southeastern United States; A. piceae canadensis, eastern Canada and New England; and 

A. piceae occidentalis, British Columbia. 

The balsam woolly adelgid was introduced into Maine and Nova Scotia in 1908 on nursery stock 

and became established on balsam fir, A. balsamea (Balch 1952). The adelgid was discovered in the 

southern Appalachians in 19551 infesting Fraser fir, A. fraseri, on Mt. Mitchell, North Carolina. Since 

then it has been found on Fraser fir in Virginia and Tennessee, and on bracted balsam fir, A. balsamea 

var. phanerolepis, in Virginia and West Virginia (Amman 1962). Balsam fir has the most extensive 

1J.S. Boyce. Memorandum of October 7, 1955, to North Carolina National 

Forests, Toecane Ranger District, Burnsville, North Carolina. Southeastern 

Forest Experiment Station, Asheville, North Carolina. As reported in Amman 

1966. 

272 
Generalized Adelgid Life Cycle 

Fertilized Eggs 

Fundatrix • nymphs 

Fundatrix • mature females 

Parthenogenetic • Eggs 

Gallicolae • nymphs 

t Emerge as alates (fly to 

secondary host) 

Parthogenetic • Eggs 

Sistens nymphs • 

(neosistentes) 

S

. • 1stens mature 

females 

• ~·~--------------~ t 

Alate sexuparae Apterous 

(fly back to oviparae 

primary host) (remain on 

4 secondary 

Sexuales host) 

Season 

Fall 

Winter 

Spring 

Summer 

Fall 

Fall 

Winter 

Spring 

Summer 

Figure 1. Holocyclic and anholocyclic life cycles of adelgids. 

range of all the North American true firs, occurring from Newfoundland to Alberta, Labrador to 

Pennsylvania; however the adelgid is only found on balsam fir in New England (as far south as New 

York), Newfoundland, Nova Scotia, New Brunswick, and Quebec (Greenbank 1970, Mitchell et al. 

1970). A separate introduction occurred in the Pacific Northwest, where the principal hosts are grand 

fir (A. grandis), subalpine fir (A. lasiocarpa), and Pacific silver fir (A. amabilis) (Mitchell 1966). 

The life cycle of the balsam woolly adelgid consists of the egg, three larval instars, and the 

adult. The first instar, or crawler stage, is about 0.4 mm in length, and is the only form capable of 

movement (Fig. 2). Within 24 to 48 hours after hatching, the crawler locates a suitable feeding site, 

inserts its stylets into the bark of the host, and transforms, without molting, into a flattened, waxfringed resting stage (neosistentes). The insect is sessile, remaining permanently attached to the 

feeding site which is usually a bark lenticel or other roughened area of the main stem, branch, twig 

node, or bud base (Bryant 1974). Dispersal occurs when the crawlers or eggs are passively transported 

by wind, birds, or other animals. The second and third instars are about 0.50 and 0.65 mm in length, 

respectively. They closely resemble the adult and are covered with secretions of waxy threads that 

appear as a dense white wool mass. The second instar through the adult are considered the sistentes. 

The adult females are about 0.80 mm in length, dark purple to black, nearly spherical, and wingless. 

As many as 248 amber-colored eggs are laid within the woolly mass. The dense woolly secretions 

provide protection for all of the life stages except the crawler (Balch 1952). The progrediens stage has 

273 
been observed in Europe and the Maritime Provinces of Canada (Mitchell et al. 1970), although it is 

rare. There are winged and wingless forms of the progredientes. The wingless form is similar to the 

sistentes, while the winged form has conspicuous membranous wings and five-segmented antennae and 

generally lack wax pores. The progrediens stage gives rise to the neosistens stage. 

The winter is passed as a dormant first instar nymph, and this generation is referred to as 

hiemosistens. Development is completed in the spring (Balch 1952, Greenbank 1970). The first instar 

nymphs of the second generation (aestivosisten) also undergo a dormant period (summer aestivation) 

ranging from 2 to 8 weeks (Amman 1969). At lower altitudes or warmer climates, additional 

generations may be produced (Arthur and Hain 1984, Mitchell et al. 1961). A third generation usually 

results from faster development, and a partial fourth may occur during years of extremely early 

development. 

The amount of damage sustained by an infested tree is related to the size of the attacking 

adelgid population, to the part(s) being attacked, and to the physiological state of the tree. Adelgids 

generally concentrate in the outer portions of tree crowns or on the main stem and large branches. 

The precise location of the infestation depends on the tree species and geographic location. Stem 

infestations usually cause more damage and tree mortality than do crown infestations. Heavy stem 

attacks give the lower bole a white-washed appearance because of the conspicuous presence of white 

woolly masses. In some cases, stem infestations may virtually disappear after a few years without 

killing the tree--this is especially true in Europe. However, many North American firs are killed within 

2 to 6 years of a sustained infestation. 

The anatomical, structural, and physiological changes in host tissue caused by an A. piceae 

infestation include the production of abnormal wood (rotholz) in the xylem tissues, an increase in 

outer bark thickness, bark resinosis and sometimes copious resin flow from within the feeding zone, 

and the production of juvabione and juvabione-like compounds. The stimulation of the cambium to 

produce rotholz is particularly intriguing, since the physical presence of the stylets only extend to the 

living bark cells. In young and thin bark tissue, the stylets occasionally reach the phloem but do not 

enter it (Balch 1952). 

Rotholz is usually reddish in color and resembles compression wood (Balch 1952, Busby 1964, 

Varty 1956). The intensity of the red coloration varies from barely noticeable to dark red. The xylem 

tissue from infested fir contains higher amounts of ray tissue (Mitchell 1967, Smith 1967), thickened 

cell walls, shorter tracheids (Doerksen and Mitchell 1965, Foulger 1968), a reduced number of 

conducting pits in the tracheids (Puritch and Petty 1971 ), and encrusted pit membranes that resemble 

those of normal heartwood (Puritch and Johnson 1971). 

Water flow through sapwood samples from infested trees was greatly reduced (Mitchell 196J), 

almost to the level of non-conduction (Puritch 1971 ). There are no distinguishable differences between 

normal heartwood and the heartwood formed as a response to adelgid attack (Puritch 1971, 1977, 

Puritch and Petty 1971). Since the cambium and ray cells are not physically damaged, it appears that 

the adelgid merely enhances the normal pattern of heartwood formation. An infestation is also 

associated with the production of chemical compounds in the sapwood (Puritch 1977). In contrast to 

uninfested trees, water transport in infested trees is limited to narrower bands of early wood and does 

not ascend as high (Mitchell 1967). The tree is in a state of physiological drought. As fluid 

movement is impaired, photosynthesis and respiration are reduced, contributing to the death of the 

host. European firs do not form rotholz in response to attack (Mitchell 1966), which may explain the 

innocuous status of the pest. 

When the periderm tissue of conifers is injured a layer of impervious tissue (Biggs 1985, Mullick 

1975) followed by necrophylactic (secondary) periderm is formed internal to the wound (Mullick and 

Jensen 1973a, 1973b ). This impervious tissue isolates the necrotic cells of the wound response from 

the unwounded portion of the stem. In a susceptible response to an adelgid infestation, the formation 

274 
one millimeter 

d 

~b 

~ 

c 

Figure 2. Life stages of the balsam woolly adelgid: a) adult with stylets 

piercing bark tissue, b) crawler, c) neosisten with wax fringe and stylets 

piercing bark tissue, and d) egg. 

of the impervious layer may be inhibited (Mullick 1975, 1977), perhaps as a result of stylet secretions. 

The wound response continues into deeper tissue layers and ultimately into the xylem, where rotholz is 

formed. By contrast, tolerant firs may complete the formation of the impervious tissue without delay 

and thus avoid any permanent damage to the underlying cells. Eventually nutrients in the outer bark 

become exhausted and the adelgid disappears leaving the tree relatively unharmed. 

The wound response of some fir, especially grand fir, Abies grandis, produces such copious 

amounts of resin that it flows down the bole. Grand firs are considered one of the more resistant 

North American fir species to adelgid attack with only 20 to 30 percent of the infested trees dying 

(Mitchell 1966). Adelgid-infested grand firs do not always produce rotholz (Puritch and Petty 1971 ), 

although the anatomical and chemical features of the xylem are altered and permeability reduced 

(Puritch 1973, 1977, Puritch and Petty 1971, Puritch and Johnson 1971). 

Also juvabione-Iike substances may be produced by the host in response to an adelgid 

infestation. The substances were not found in uninfested fir, nor were they found in infested fir except 

in the vicinity of the adelgid (Puritch and Nijholt 1974). Perhaps the juvabione-Iike compounds 

interfere with the metabolism of the insect and render the tree resistant to a prolonged infestation. 

We have reviewed the general life history of adelgids that attack spruce and fir, focusing on an 

adelgid introduced into North America, the balsam woolly adelgid. Research into the interactions of 

the adelgid with its new hosts has shown that the infested trees respond, in varying degrees, by the 

production of rotholz in the xylem, wound periderm in the bark, resins, and juvabione-Iike substances. 

275 
The objective of our research at North Carolina State University has been to clarify the importance of 

each of the reaction components (rotholz, wound periderm, resin, and juvabione-like substances) to the 

tolerance or susceptibility of Fraser fir to the balsam woolly adelgid. This paper will review that work 

and propose a hypothesis for the cause of tree susceptibility or tolerance. 

METHODS 

Most of these studies were conducted on Fraser fir, Abies fraseri, in the southern Appalachians 

of North Carolina. However, some comparative studies were also conducted on European silver fir, 

A. alba, in the Black Forest of Germany. 

Rotholz Formation and Water Potential 

Several methods were used to determine the presence of rotholz. The first was wood coloration. 

Wood cores were taken from opposite sides of trees. When a growth ring from both cores showed a 

high proportion of latewood, giving it a reddish coloration, the ring was considered to contain rotholz. 

Some cores were also treated with perchloric acid (a heartwood indicator) to enhance the difference in 

coloration. Other cores were examined by electron microscopy. Rotholz is anatomically similar to 

compression wood (Balch 1952), having thick-walled tracheids which are circular (rather than 

rectangular) in cross-section (Doerksen and Mitchell 1965, Timell 1986), and encrusted pit membranes 

which appear similar to those of heartwood (Puritch and Johnson 1971). 

Water potential of individual trees was measured using a Scholander pressure chamber 

(Scholander et al. 1965) and all readings were taken at dawn. When necessary, extension clippers were 

used to remove a branch from the upper crown and a 2-year-old twig was cut from the branch for use 

in the chamber. 

Sapwood flow rates were measured through Fraser fir stems previously infested by the balsam 

woolly adelgid and containing rotholz. Four pairs of Fraser fir were cut and removed from an infested 

Christmas tree plantation. Each pair included one tree which had been heavily attacked by the adelgid 

and a second tree which did not show symptoms of a heavy infestation. Ten-em long bole sections 

were placed with the bottom portion in a reservoir of distilled water, and a partial vacuum pressure of 

10 psi was applied to the upper portion. The amount of water drawn through the sample during two 

consecutive 2-minute intervals was recorded. Water dyed with food color was then drawn through the 

sample at 27 psi. Flow rates were calculated on a per unit area of sapwood basis. Sapwood was 

defined to include all wood except heartwood. 

Wound Periderm and Bark Thickness 

The formation of wound periderm was evaluated by artificially wounding individual trees using a 

scalpel to make several shallow cuts (5 mm x 3 mm x 1 mm deep) in the bark surface. Trees were 

examined for suberized impervious tissue by removing a circular bark plug (with the wound in the 

center) about 3 weeks after wounding. The formation of impervious tissue was determined by the F-F 

test (Mullick 1975). The bark plugs are held phloem side down in a 2 percent solution of FeC13 for 3 

days, and then in a 4 percent solution of KFe(CN)6 for an additional 3 days. After drying, a radial 

cut through the bark plug exposes a light brown zone of necrotic tissue surrounding the wound. 

Immediately below this tissue is a thin layer of dark brown tissue, the suberized impervious tissue. 

The remainder of the plug will be colored dark blue. If the impervious layer is not formed, the entire 

sample will be dark blue. 

Outer bark thickness was determined also using the F-F test. Unwounded plugs were taken 

from two sides of a tree. After staining, the samples were cut, and the maximum depth of any 

impermeable layer present (i.e. outer bark) was measured. 

276 
Monoterpene Analysis 

We quantified the volatile fraction of resin, the monoterpenes, that was present within the 

necrotic tissue surrounding an artificial wound produced as described above. The monoterpenes found 

in healthy Fraser fir have been identified (Zavarin and Snajberk 1965, 1972, Thor and Bennett 1974), 

but there was no information concerning the monoterpene fraction of wounded tissue. 

Wounded trees were sampled using a cork borer (dia. 11 mm) to remove a circular bark plug 

from the wound surface. All samples were placed in individual vials containing 4 ml of n-pentane, 

placed in a container of dry ice and taken to the laboratory and held at OOC until analyzed. Control 

samples of unwounded tissue were handled in the same manner to determine the constitutive 

monoterpene composition. 

The monoterpene content of each sample was analyzed by gas chromatography using one 

microliter of paracymene as an internal standard. All monoterpenes were identified by comparing their 

retention times with that of known standards. The amount of each monoterpene was quantified using 

a recording integrator. After this analysis, the dry weight of each bark sample was determined. 

Juvabione Analysis 

Juvabione analyses have been reported earlier (Puritch and Nijholt 1974, Manville 1975, 1976, 

Manville and Bock 1977, Manville and Kriz 1977). However, our procedures were different. We 

analyzed air-dried 5/8 inch woodcores rather than cross-sections of felled trees. The most recent 

annual ring and any annual rings showing evidence of rotholz were analyzed. The wood sections were 

ground up and subjected to a So:mlet extraction (24 hr) with methanol. The extract was eluted 

through a C18 Waters sep-pak with 10 ml of methanol, and then analyzed by capillary gas 

chromatography. The retention times were compared to those of pure samples of extracts of Douglasfir supplied by Dr. John Manville (verified by GC-MS). 

Genetic Variations of Fraser Fir 

Because of the wide variation in mortality caused by the balsam wooly adelgid within the natural 

range of Fraser fir, a related study assessed the genetic architecture of the southern Appalachian 

endemic Fraser fir by analyzing seven polymorphic allozyme loci found in five major mountain 

populations. Mature mother trees and their respective progeny were sampled in groups of 5 to 10 at 

the peaks of the mountains, and at other representative locations within populations. Samples 

consisted of cones with ripe seed. 

Cleaned seed were germinated on moist filter paper and then subjected to electrophoretic 

analysis. Megagametophytes and embryos were excised from the seed coat, crushed separately, and 

inserted into the vertical slice of a gel. Of the approximately 25 enzymes tested in preliminary trials, 

12 were chosen for scoring because of their good resolution in embryos and gametophytic, or their 

polymorphic character. 

RESULTS AND DISCUSSION 

Rotholz Formation and Water Potential 

Although rotholz production is a common occurrence in infested fir species of North America, 

not all infested trees show the visual signs of rotholz. However, the lack of any visible indications of 

rotholz does not necessarily indicate that the xylem has been unaltered by the infestation. Heavily 

infested grand firs, grown as exotics in Scotland, were found to contain no visible evidence of rotholz, 

yet the sapwood of these trees was only one-twentieth as permeable as sapwood sampled from nearby 

277 
uninfested trees. The adelgid-altered wood stained the same color as heartwood (Puritch 1971). The 

reduced permeability was due to a combination of tracheid pit membrane encrustation and accelerated 

embolism (Puritch and Johnson 1971, Puritch and Petty 1971 ). 

Rotholz formation in infested Fraser fir was evaluated by studying wood cores taken from six 

sites near Mt. Rogers, Virginia, and five sites in the Black Mountains of North Carolina. Average 

adelgid densities were higher for trees sampled at Mt. Rogers. At moderate-to-high infestation 

densities, the proportion of trees producing rotholz was similar between locations. However, a 

significantly higher proportion of trees from the Black Mountains produced abnormal wood when 

lightly infested. 

Pressure chamber measurements, made on cut shoots of Fraser fir, add additional evidence that 

adelgid infestations might interfere with water transport through the sapwood. Measurements taken in 

June showed that infested trees at Mt. Mitchell and Roan Mountain, North Carolina, had lower xylem 

pressure potentials (an indication of poorer water status) than uninfested controls, while the infested 

and uninfested trees at Mt. Rogers, Virginia, did not differ from one another. In mid-summer, there 

were no significant differences at any site. However, infested trees at all locations showed lower water 

potentials than uninfested trees when measured in September (Arthur and Hain 1986). Increment 

cores taken from infested trees at all three sites contained visible rotholz, and nearly all cores from 

uninfested trees at Mt. Mitchell also contained rotholz. This suggests that the uninfested trees at 

Mt. Mitchell may have recovered from an earlier infestation. As September was a low-rainfall month 

in the southern Appalachians during this study, these results may indicate that the physiological effects 

of adelgid-caused damage are more severe during periods of low rainfall. 

In a comparative study in the Black Forest of Germany, xylem and phloem potential 

measurements were made on ca. 10-year-old silver fir infested with a closely related adelgid, Adelges 

(= Dreyfusia) nordmanniana, which infests branches and twigs. Trees were classified as uninfested, 

lightly infested, and heavily infested. Table 1 shows that both the phloem and xylem potential readings 

of the infested trees were considerably higher than that of the uninfested. In fact, the phloem of many 

of the infested trees had liquid oozing out of just one or two spots rather than the entire phloem area. 

When tested for rotholz with perchloric acid, many of the smaller twigs tested positive. 

A. nordmanniana was introduced into the Black Forest and is considered a pest. It is also capable of 

causing rotholz formation on the thin-barked twigs, while the native A. piceae does not cause rotholz 

formation on the thicker-barked boles of silver fir. 

When sapwood flow rates were measured through Fraser fir stems previously infested by the 

adelgid, areas of rotholz generally did not transport dye. Rotholz inclusion is associated with reduced 

sapwood permeability and an increase in the proportional area of heartwood (Hollingsworth and Hain, 

Table 1. Water potential readings of Abies alba infested with Dreyfusia 

nordmanniana 

Water potential (-bars) 

Degree of infestation Xylem Phloem 

Heavily infested (n - 16) 10.09 ± 3.27 1.46 ± 1.06 

Lightly infested (n - 10) 7.95 ± 1.96 1.75 ± 2.55 

Uninfested (n - 15) 8.03 ± 2.67 0.73 ± 0.44 

278 
unpubl. data). These results lend support to the hypothesis that rotholz leads to water stress in the 

crowns of infested trees. 

Wound Periderm and Bark Thickness 

Adelgid attack causes chemical and structural changes within the tissue of susceptible hosts 

(Balch 1952). Initially the number and size of bark parenchyma cells increase within the area 

surrounding the insect's stylets. Within a year, these enlarged cells become surrounded by purplish 

cork cells which are produced by secondary phellogen. The parenchyma cells disintegrate, and the area 

becomes infiltrated with resin and completely enclosed within cork tissue. In heavily infested stems, 

this secondary cork cambium forms two or more millimeters beneath the surface of the bark, forming a 

localized, thickened layer of dead outer bark cells which physically prevents feeding by future 

generations. 

The response described above is typical of conifers injured by biotic or abiotic factors. It serves 

to isolate the damaged area from the living tissues of the bark, while adding additional layers of 

protection in the damaged area. Many woody plants (Mullick 1977) exhibit this type of non-specific 

response when living bark cells are damaged. 

In fir trees, the wound response initially involves the formation of a layer of suberized 

impervious tissue (Mullick 1975) to wall-off the damaged tissue, followed by the formation of a 

reddish-purple sequent (necrophylactic) periderm internal to the impervious layer. To determine if 

inherent variation in the formation of the layer of suberized impervious tissue could account for the 

observed mortality patterns of Fraser fir in the southern Appalachians, we tested 89 firs from seven 

locations for the complete formation of the suberized impervious tissue at artificial wound sites. The 

F-F test (Mullick 1975) showed that all the trees except one formed the impervious layer in a time 

period that was considered normal (3 weeks) during the growing season, with no delays due to tree 

age, location, or presence of balsam woolly adelgids. 

There are a few instances where specific chemicals have been associated with a balsam woolly 

adelgid attack. The saliva of the adelgid contains auxin-like compounds (Balch et al. 1964) and 

pectinase (Adams and McAllan 1958). A juvabione-like substance, todomatuic acid, was found in the 

bark of infested grand fir (Puritch and Nijholt 1974). To determine the effect of these chemicals on 

the formation of the suberized impervious tissue at wound sites, we artificially wounded 86 fir trees 

(including 10 European silver fir planted at Mt. Mitchell) at three locations in the southern 

Appalachians. The wounds were treated with either napthalene acetic acid (NAA), pectinase, or 

todomatuic acid (Arthur and Hain 1985). None of the chemicals delayed formation of the impervious 

tissue. 

Observations on other fir species indicate that outer bark, formed in response to attack by the 

balsam woolly adelgid, is frequently associated with recovery of infested trees (Brower 1947, PschornWalcher and ZwOifer 1958, Schooley and Bryant 1978). Apparently the outer bark forms a physical 

barrier to adelgid feeding, or forces the insect to feed on other portions of the tree. Of 94 trees 

measured for bark thickness at Mt. Rogers, and 99 at Mitchell, a higher proportion of infested trees 

had outer bark thickness greater than 1.5 mm (the average length of a balsam woolly adelgid stylet) in 

comparison to uninfested trees. This was especially true of trees with a high infestation density and 

for trees with old wool only. Trees with old wool were recently infested (the woolly masses had not 

washed off yet), but not currently infested. 

There was some indication that the "outer bark" detected in the Mt. Mitchell trees (defined by 

its impermeability to staining solutions) was not completely impermeable to the passage of moisture 

from the inner bark. When a new periderm layer is formed internal to the old one, all of the bark 

tissue between the two layers should gradually desiccate, becoming hard and compressed. Because of 

its distinct texture, this tissue is easily identified, and was classed as "dry outer bark" at the time we 

279 
measured the thickness of the impermeable tissue. From Mt. Rogers, there were 23 trees which 

contained a measurable amount of outer bark, and 16 of these also contained "dry outer bark" as a 

proportion of the total outer bark thickness. By contrast, only 8 of 37 Mt. Mitchell trees with outer 

bark also contained "dry outer bark." 

Average thickness of the dry outer bark was considerably greater for the silver fir trees from 

Germany, regardless of infestation class, than for Fraser fir trees of the southern Appalachians 

(Hollingsworth and Hain, unpubl. data). Silver fir trees generally contained more moist outer bark as 

well. It seems probable that silver fir trees naturally produce more outer bark than Fraser fir. An 

alternative explanation is that many of the silver fir studied may have formed the outer bark in 

response to previous infestations. 

Monoterpene Deposition 

The bark of 22 mature Fraser fir from Mt. Mitchell and Mt. Rogers was artificially wounded. 

Two to six weeks after wounding, wound tissue and unwounded tissue were sampled and analyzed for 

monoterpenes. 

The results of the bark wound reaction study showed that there were no differences in total 

monoterpene content between wound tissue and normal bark tissue at either Mt. Mitchell or 

Mt. Rogers. However, there were differences between the two sites. Trees from Mt. Rogers had lower 

amounts of delta-3-carene relative to Mt. Mitchell. The variation between trees at Mt. Mitchell (which 

probably reflects historical harvesting and planting practices) could indicate differences in susceptibility 

to adelgid attack. Because Mt. Rogers trees have experienced little adelgid-caused mortality, it has 

been hypothesized (Arthur and Hain 1987) that those Mt. Mitchell trees that more closely resemble 

Mt. Rogers trees (and may in fact be a Mt. Rogers seed source) are more tolerant of an adelgid 

infestation. 

In a similar study in Germany's Black Forest, monoterpene composition of wounded and 

unwounded tissue was compared between infested trees from a low elevation site and healthy and 

declining trees at a high elevation site. The cause of the decline at the high elevation site was unclear 

(perhaps it was influenced by atmospheric deposition) but none of the trees showed any sign of a 

balsam woolly adelgid infestation. 

As seen in Fig. 3, the amount of monoterpenes found in the phloem tissue was considerably 

higher in the trees from the infested site. This was especially true for the wounded tissue. The 

monoterpene composition (Fig. 4) for the wounded tissue of the infested trees was similar to that of 

the wounded tissue of the declining trees at the high elevation. The amount (Fig. 5) of limonene in 

the unwounded tissue of the infested trees was also very high compared to the other trees. 

It appears that the silver fir of the Black Forest, as opposed to Fraser fir, do respond to 

wounding of the phloem tissue by an accumulation of monoterpenes around the wound site. 

It is not clear whether monoterpenes contribute to the tolerance mechanisms of fir trees infested 

by the balsam woolly adelgid. However, for other conifer species, monoterpene contents are thought to 

be important for host resistance to a number of insect pests and diseases (Rockwood 1973, Shrimpton 

1973). 

Juvabione 

In addition to monoterpenes, some members of the genus Abies produce sesquiterpenoids which 

act as insect juvenile hormones (Slama and Williams 1965). Two such compounds, todomatuic and 

dehydrotodomatuic acids, have been identified from Pacific silver fir and grand fir infested with the 

adelgid (Puritch and Nijholt 1974). These compounds were found only in the vicinity of attack and 

280 
-C) 

--::1. 

-

Q) 

c.. 

E 

rn 

C/) 

en 

Q) 

c 

Q) 

a. 

~ 

Q) 

0 

c 

0 

~ 

rn 

...... 

0 

0.8 

0.6 

0.4 

0.2 

~ 0.0 

Decline-w Decline-c Healthy-w Healthy-c 

Tree Status 

infested tnfested-c 

Figure 3. Total monoterpenes of European silver fir in the Black Forest of 

Germany. Decline-W- wound tissue from an uninfested declining tree, 

Decline-C ~ unwounded control tissue, Healthy-W- wound tissue from an 

uninfested healthy tree, Healthy-C -unwounded control tissue, Infestedwound tissue from an infested tree, and Infested-C - unwounded control tissue. 

were not present in uninfested trees. Todomatuic acid and juvabione have been isolated from seedlings 

of infested Fraser fir (Sanchez, unpubl. data). 

The trees at the two sites in the Black Forest were also examined for the presence of juvabione 

and todomatuic acid (Table 2). Both compounds were detected but in very small amounts, especially 

the todomatuic acid. The concentration of these compounds was about 100-fold less than that detected 

in the infested Fraser fir seedlings (Sanchez, unpubl. data), and about 10-fold less than that detected in 

some of the infested mature grand and Pacific silver fir (Puritch and Nijholt 1974). However, the 

compounds were detected in the mature European silver fir, even in uninfested trees. 

It has been hypothesized that juvabione-related compounds may interfere with adelgid 

development (Puritch and Nijholt 1974). The effective level of concentration, however, is unknown. 

Genetic Variation of Fraser Fir 

This study (Ross 1988) assessed the genetic architecture of Fraser fir throughout its restricted 

geographic range by analyzing seven polymorphic allozyme loci. The five major mountain populations 

differed slightly but significantly from each other with respect to allele frequency for both mature tree 

and progeny populations. The Mt. Rogers trees had the most extreme allele frequencies and appear to 

be an outlier among the five mountain populations. These differences may be due to local, restricted 

281 
Table 2. Presence of juvabione and todomatuic acid in Abies alba 

Bark thickness ul/g ± SE 

Type Age ± SE MM ± SE Juvabione Todomatuic acid 

Declining 96 ± 8 8.25 ± 1.66 1.60 ± 0.38 0.13 ± 0.20 

Healthy 91 ± 5 9.39 ± 1.68 1.34 ± 0.13 0.03 ± 0.02 

Infested 55 ± 7 6.28 ± 0.96 1.88 ± 0.52 0.01 ± 0.01 

mating and genetic drift. Therefore, the distinctiveness of the Mt. Rogers fir trees is demonstrated 

genetically as well as entomologically with regards to adelgid tolerance. However, it has not been 

demonstrated that the genetic distinctiveness is in any way related to adelgid tolerance. 

SUMMARY AND HYPOTHESIS 

The balsam woolly adelgid's life cycle is anholocyclic with parthenogenetic reproduction on fir 

trees only. The adelgid is native to the fir trees of central Europe but has been introduced into North 

America. European firs are not seriously affected, but North American firs frequently experience either 

crown .dieback or tree death, or both. Fraser fir, in the southern Appalachians, is one of the most 

susceptible North American species to an adelgid infestation. Research into the interactions of the 

adelgid with its new North American hosts has shown that infested trees respond by the production of 

rotholz in the xylem tissue, wound periderm in the bark tissue, resins, and juvabione substances. The 

objective of this paper has been to clarify the importance of each of the reaction components to the 

tolerance or susceptibility of Fraser fir to the adelgid. Comparisons with European silver fir were also 

made, and the genetic architecture of the major mountain populations of Fraser fir was examined. 

Balsam woolly adelgid infestations interfere with water transport through the sapwood and 

undoubtedly interfere with phloem transport as well. Whether rotholz is visible or not, water potential 

measurements were lower in infested trees. In trees with rotholz, dye transport within the rotholz zone 

did not occur and there was an increase in the proportional area of heartwood. A significantly higher 

proportion of trees from the Black Mountains produced rotholz when lightly infested than did trees 

from Mt. Rogers, suggesting a greater sensitivity to an adelgid infestation in some mountain 

populations of Fraser fir. 

Outer bark formed in response to attack by the balsam woolly adelgid appears to be associated 

with recovery of infested trees. Infested trees, at both Mt. Mitchell and Mt. Rogers, had a higher 

proportion of trees with an outer bark thickness greater than 1.5 mm. However, a higher proportion 

of Mt. Rogers trees contained "dry outer bark" as a proportion of the total outer bark thickness. The 

average thickness of the dry and moist outer bark of the silver fir trees in Germany was considerably 

greater than that of Fraser fir, regardless of infestation class. This suggests that the formation of outer 

bark, especially dry outer bark, is an important tolerance mechanism for mature trees infested by the 

adelgid. 

While differences in monoterpene composition of bark tissue did exist between Mt. Mitchell and 

Mt. Rogers trees, there was no significant accumulation of monoterpenes in wounded bark tissue. This 

is in contrast to the silver fir of the Black Forest where wound tissue surrounding an artificial wound 

had a significantly higher accumulation of monoterpenes than unwounded tissue, especially in currently 

infested trees. 

282 
c:: 

0 

= 

en 

0 

c. 

E 

0 

(.) 

eft. 

0 a-pinene 

FB camphene 

• B-pinene 

~ 63-carene 

0 myrcene ml limonene 

EJ a-phellandrene 

Decline-w Decline-c Healthy-w Healthy-c Infested lnfested-c 

Tree Status 

Figure 4. Composition of monoterpenes of European silver fir in the Black 

Forest of Germany. See Fig. 3 for description. 

Juvabione-related compounds have been found in several fir species and may cause abnormal 

adelgid development. In some North American fir species the compounds were only found in infested 

trees. Infested Fraser fir seedlings had extremely high quantities of these compounds. Both infested 

and uninfested mature silver fir of Germany had detectable amounts of the chemicals, but in very low 

quantities. If these compounds do interfere with adelgid development, the effective concentration level 

is not known. 

The balsam woolly adelgid studies in the southern Appalachians have demonstrated that the fir 

population at Mt. Rogers is unique with regards to adelgid/fir interactions. A genetic study of allele 

frequencies has also demonstrated the distinctiveness of the Mt. Rogers fir population. The 

Mt. Rogers trees had the most extreme allele frequencies and appear to be an outlier among the fir 

populations of the southern Appalachians. 

Although our knowledge of the balsam woolly adelgid/Fraser fir interaction is incomplete, we 

know enough about the system to offer the following hypotheses about susceptibility, resistance, and 

tolerance of fir to an adelgid infestation. 

In a susceptible fir there is an inadequate response tissue to the infestation within the bark. 

There is no immediate accumulation of monoterpenes or juvabione-related compounds, and an 

inadequate accumulation of outer bark. Both the phloem and the current xylem rings become nontranslocating because of chemical and structural changes within the tissue. Continuous infestation over 

a period of years results in accumulation of non-translocating tissue that eventually kills the tree, 

especially during periods of drought. 

283 
0.50 

-C) 

;_ 0.40 

-

li a-pinene 

Fa camphene 

• B-pinene 

m ~3-carene 

D myrcene m limonene 

I?.J a-phellandrene 

Decline-w Decline-c Healthy-w Healthy-c Infested lnfested-c 

Tree Status 

Figure 5. Amounts of monoterpenes of European silver fir in the Black Forest 

of Germany. See Fig. 3 for description. 

In a resistant or tolerant fir there is a rapid accumulation of monoterpene and juvabionerelated compounds surrounding the invasion site. In mature trees the chemical accumulation serves to 

inhibit survival and development of the adelgid. In younger trees, especially seedlings, the 

accumulation of juvabione-related compounds is so high that abnormal adelgid development prevents 

the insect from successfully reproducing. Older trees, which accumulate less juvabione-related 

compounds, begin to produce secondary periderm and a thick layer of outer bark. As the outer bark 

thickens and dries, it becomes unsuitable as an adelgid substrate. The insect either abandons the host, 

or abandons that part of the host, to infest another tree or another part of the same tree. If the 

process occurs rapidly, minimum damage is inflicted and the tree survives. 

Future work will examine the above hypotheses in greater detail. 

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287 
SIGNIFICANCE OF PHYTOHORMONES 

IN SIBERIAN LARCH-BUD GALL MIDGE INTERACfiON 

RIDA M. MATRENINA 

V.N. Sukachev Institute of Forest and Wood 

Siberian Branch of the U.S.S.R. Academy of Sciences 

Krasnoyarsk 660036 U.S.S.R. 

INTRODUCTION 

Interrelations of the bud gall midge and the Siberian larch are of scientific and practical interest 

because of the bud gall midge's role as a plant endoparasite. We know that attack by the gall midge 

sets off a reaction in the entire plant. Invasion by the insect results in a certain interaction between 

physiological mechanisms of the insect and the plant which leads to a complex range of interdependent 

shifts in the metabolism of the tree, the final result depending on the character of those shifts. The 

reactions of both the plant and the insect are determined both by genetic factors and by environmental 

conditions. 

The bud gall midge has long been considered a pest of the larch in Siberia even though it does 

not cause significant mortality among the trees. Some papers have been written on the effect of the 

gall midge on morphological and physiological parameters of the larch (lsaev et al. 1988). Damage to 

the larch by the bud gall midge involves reduction of the assimilative apparata. The gall midge infests 

the buds of the brachyblasts. Where the eggs have been laid under the cover scales of the buds, a gall 

appears, functioning during one season in which the whole cycle of insect development takes place. 

MATERIALS AND METHODS 

The balance of phytohormones in the plant, which is upset by the insect, has not been studied 

enough, though hormonal changes in damaged plant tissue have been recorded. In our study, 

phytohormone dynamics were examined in the needles, buds, and galls from the time of needle 

initiation up to the time of their yellowing and fall in the autumn, taking into account insect 

development stages, and tree differentiation according to the rate of pest invasion. To study the 

phytohormones, we used a set of methods including extraction, purification, chromatography, and 

biological activity tests. Identification by bioassays was made according to the growth of pieces of 

wheat coleoptiles and larch and lettuce hypocotyls, the capacity to produce color reactions, 

luminescence in the UV-light, and rechromatographing in different systems of solvents. 

RESULTS 

If larch is chronically infested by the gall midge, an increase occurs in the quantitative and 

qualitative composition of indole compounds and in their biological activity. The levels of endogenous 

auxins depend on the ratio of their synthesis and inactivation rates. The activity of indoleacetic oxidase 

in different parts of the larch does not change considerably as a result of midge invasion. Activity of 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

288 
the gibberellin-like and cytokinin-like substances increases, however. The rise in the activity of these 

phytohormones correlates with the start of pathological growth of bud tissue in the infested trees. 

Their maximal activity coincides with the period of intensive growth and formation of the gall. A 

concomitant accumulation of abscisic acid inhibitors occurs during the ending of growth. Chronically 

infested trees complete their vegetation cycle with a minimum of growth-promoting substances, leading 

to retardation of needle flushing in the spring. 

Gall tissue developing in response to insect infestation is characterized by a great variety and 

activity of growth-promoting substances. The greatest amount of natural activators is found in galls 

during the first 10 days of July, when the growing process is intensive. At the end of vegetative 

growth, the growth-promoting activity of the gall extract is reduced by nearly half. Gall tissue is 

hormone-dependent, i.e. it cannot synthesize phytohormones while in tissue culture, as is the case for 

tumor tissue. Formation of gall tissue is a response by the tree to the midge infestation and is a 

necessary condition for normal development of insect larvae. Mechanical destruction of the gall causes 

mortality of the insect larva. 

Increases in the activity of phytohormones occur at definite times, corresponding to the first and 

second larval instars. Invading the tissue of the host plant, the larva changes the plant's metabolic 

pattern. By using the attractive capacity of auxins, the midge larva attracts and accumulates mobile 

metabolites in the gall tissue. Thus one can see that gall-forming insects can cause shifts in the 

hormonal balance of the host plant, changing the content of its natural regulators. 

DISCUSSION AND CONCLUSIONS 

Most believe that whatever agent has caused the pathological tissue to form (mutations, 

infections by fungi, bacteria, insects), does so by eliciting changes in the activity or synthesis and 

degradation of plant hormones. Increases in auxins can be related to the accumulation of auxin 

protectors in the tissues and organs of the larch tree. The role of protector is performed by the 

phenols of the ortho-diphenol type, which serve as inhibitors of, IAA disintegration. At the same time, 

some authors suggest that in natural conditions, loss of resistance to pathological growth is connected 

with a drop in the level of endogenic gibberellic acid or decreased sensitivity to it. Cytokinins are 

found in various parasitic organisms and seem to play a role in the development of anomalous tissue. 

Growth promotion based on elevated cell division and/or growth and a rise in mitotic activity is 

regulated by phytohormones. The specific effect of the bud gall midge on the buds connected with the 

gall occurs through induction. Induction starts the process (under the influence of the phytohormone) 

and does not occur in cells in the absence of the requisite hormones. In the case of gall tissue 

formation, two mechanisms, induction and promotion, operate together. Induction of pathologic 

growth is caused by secretory exometabolites of the bud midge larva. In line with the classic theory of 

mechanisms of realization of genetic information in the bacterial cell, Bonner (1967) suggested that 

hormones function by activating the genes which have previously been suppressed. Experimental data 

however, do not support this hypothesis. Though accumulation of natural growth stimulators and 

inhibitors in the larch tree damaged by the midge does not constitute direct evidence for the 

participation of phytohormones in the induction of anomalous growth, it does indicate that a change in 

the hormonal status of the host plant has occurred under the impact of the insect. 

One may conclude, then, that the network of protective reactions to the pathologic growth 

stimulated by the bud midge is based on a shift in the balance of natural stimulators and growth 

inhibitors, reflecting complex interrelations between the plant and the insect. 

289 
LITERATURE CITED 

BONNER, J. 1967. Molecular biology of development. Moscow. 179 p. 

ISAEV, AS., BARANCHIKOV, Y.N., and MALUTINA, V.S. 1988. The larch gall midge in seed 

orchards of South Siberia, p. 30-44. In Berryman, AA, ed. Dynamics of Forest Insect 

Populations. Plenum, New York. 

290 
MANIPULATION OF HOST PLANT BIOMASS 

ALLOCATION AND RESOURCE REGULATION 

BY THE LARCH BUD GALL MIDGE 

YURIN.BARANCHIKOV 

V.N. Sukachev Institute of Forest and Wood 

Siberian Branch of the U.S.S.R. Academy of Sciences 

Krasnoyarsk 660036 U.S.S.R. 

INTRODUCTION 

Intensive herbivory may influence the resources available to the next generation of herbivore in 

three ways: quantity may decrease, be unchanged, or increase. There are now two good examples of 

the last possibility. One of them concerns Monochamus beetles on firs in Siberia (lsaev et al. 1984), 

and the other a galling sawfly on willow in Arizona (Craig et al. 1986). The highly intimate and 

sedentary way of life of galling insects should predispose them to evolve the means to manipulate their 

hosts. Therefore, it is not surprising that a third example which we report herein deals also with a 

gallmaker. 

The larch bud gall midge, Dasyneura rozkovi Mamaev et Nykolsky, forms galls in the vegetative 

buds of Siberian larch shoots, causing gall-bearing buds to die. In South Siberia during persistent and 

heavy infestations, trees may lose up to 95 percent of their buds. Such trees produce no flower buds, 

so commercial seed production on infested seed orchards is impossible (lsaev et al. 1988). 

RESOURCE REGULATION 

Our data deal with sixty, 45-year-old sample larch trees in a single seed plantation near 

Krasnoyarsk which varied considerably in the level of gall infestation. Though the increasing level of 

bud infestation decreases the number of flowers, it does not influence the current year's crown biomass 

production. Forming galls appear to function as metabolic sinks working as "redirectors" of tree 

resources. The tree translocates nutrients to branch periphery where last year's infested shoots are 

situated. The biomass of newly formed galls is negatively correlated with the biomass increment of 

older branches. In spite of a great shortage of living buds on 3- to 4-year-old shoots, the infestation 

level does not influence the total biomass of needles on the branch. This is because the needles of 

galled buds are much longer than those of ordinary buds on the same tree: the weight of a single 

needle may increase by 40 percent and the number of needles in the cluster by 11 percent. 

The quantity of galls per shoot correlates positively with the incidence of shoot tip mortality and 

increasing lateral branching. Newly formed shoots have 10 to 15 percent higher bud density per shoot 

and increase simultaneously with the level of tree infestation. On galled larches, the growth rate of 

gall midge population density is limited only by the number of newly appearing buds. So in our case 

we have an example of resource regulation by the herbivore, i.e. the maintenance of higher food base 

BARANCHIKOV, Y.N., MATrSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

291 
by the gall midge that impacts immediately the subsequent generation of the same midge population on 

the same individual plant. 

There is no evidence of induced defenses against gallmaker by the larch even though midge 

infestation has a large impact on tree growth and reproduction. The reaction of larch to defoliation 

and shoot tip mortality is unspecific: increased branching and bud density following severe defoliation 

by needle-chewing insects and frost damage (Pleshanov 1982). By redirection of intershoot supplies of 

nutrients, the gallmaker stops the apical dominance in the shoot system, and in this way simply 

stimulates dormant meristems, i.e. provokes the process of general response to damage in larch trees 

(Haukioja et al. 1990). 

LITERATURE CITED 

CRAIG, T.P., PRICE, P.W., and ITAMI, J.K. 1986. Resource regulation by a stem-galling sawfly on the 

arroyo willow. Ecology 67: 419-425. 

HAUKIOJA, E., RUOHOMAKI, K., SENN, J., SUOMELA, J., and WALLS, M. 1990. Consequences 

of herbivory in the mountain birch (Betula pubescens ssp. tortuosa): importance of the functional 

organization of the tree. Oecologia 82: 238-247. 

ISAEV, AS., KHLEBOPROS, R.G., NEDOREZOV, D.V., KONDAKOV, Y.P., and KISELEV, V.V. 

1984. Population dynamics of forest insects. Nauka, Novosibirsk. (In Russian.) 

ISAEV, AS., BARANCHIKOV, Y.N., and MALUTINA, V.S. 1988. The larch gall midge in seed 

orchards of South Siberia, p. 29-44. In Berryman, AA, ed. Dynamics of Forest Insect 

Populations. Plenum, New York. 

PLESHANOV, AS. 1982. Insects defoliating larch forests in East Siberia. Nauka, Novosibirsk. 

(In Russian.) 

292 
GALL MIDGES (DIPTERA: CECIDOMYIIDAE) 

IN FOREST ECOSYSTEMS 

MARCELA SKUHRA V.A 

Institute of Entomology, Czechoslovak Academy of Sciences 

Branisovska 31, 370 05 Ceske Budejovice, Czechoslovakia 

INTRODUCTION 

The family Cecidomyiidae is one of the largest of the Diptera. Gall midges are small, 

inconspicuous flies, but they may be very important both in forest ecosystems and in agroecosystems. 

Many phytophagous gall midge species attack forest trees, and some of them can be serious pests, such 

as the Dasineura rozhkovii Mamaev and Nikolsky, which develops in bud galls of Larix sibirica Ledeb 

(lsaev et al. 1988). More than 1,200 species in 125 genera are known to occur in the Nearctic Region 

(Stone et al. 1965), and about 2,200 species in 300 genera occur in the Palearctic Region (Skuhrava 

1986). It has been estimated that the world fauna of gall midges includes four or five thousand 

species. 

Adult gall midges have small bodies, usually only 0.5 to 3 mm long, rarely up to 8 mm long, 

and long antennae. Adults do not take food and therefore cannot cause damage to humans in any 

way. The larvae of gall midges feed and develop in various environments. On the basis of larval 

feeding habits, gall midges may be divided into three ecological groups: the mycophagous 

( = fungivorous), the phytophagous, and the zoophagous (Skuhrava et al. 1984). The majority of 

described species belong in the group of phytophagous gall midges, the larvae of which develop in, or 

on, various organs of many host plant species, where they feed by sucking sap from the tissues. Many 

of them induce development of some type of abnormal plant growth, called galls. , The larvae of gallproducing species develop on most plant parts: roots, stems, vegetative tops, leaves, flowers, and fruits. 

Gall midges usually have only one generation per year, although some species have two or more 

generations per year. Adults have very short lives, sometimes only several hours long, sometimes 1 to 

4 days. Males usually perish shortly after mating, females very soon after oviposition. The typical life 

<.:ycle begins early in the spring with emergence of the adults either from the gall or from the soil 

where they hibernate as larvae. Females lay their eggs on the surface of the organs of the host plants. 

Galls develop and the larvae develop inside them, sucking sap. Development of the larvae from 

hatching to maturity (three or four stages) requires usually 2 or 3 weeks. Many species drop to the 

soil, where they hibernate. Larvae of other species live in their galls through pupation. 

Gall Midges as Forest Pests 

Barnes (1951) has reviewed of about 240 gall midge species associated with coniferous and 

broad-leaved trees in the world. The larvae of 80 species develop on various species of 14 genera of 

coniferous trees, making galls on buds, terminal shoots, needles, fruits, seeds, and cones, or living under 

bark, in resin masses, in scolytid burrows, and in aphid galls. In Europe only seven species may be 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

293 
considered serious pests: Thecodiplosis brachyntera Schwagr. on needles of Pinus silvestris L and 

P. mugo Turra, Resseliella piceae Seitner on seed of Abies alba Mill., Plemeliella abietina Seitner on 

seed of Picea excels a Link., Dasineura kellneri Henschel ( = Dasineura laricis (F. Low 1878]) on bud of 

Larix decidua Mill., Paradiplosis abietis Hubault on needles of Abies alba Mill., Taxomyia taxi Inchbald 

on terminal buds of Tarus baccata L., and Janetiella siskiyou Felt ( = Craneiobia lawsonianae de 

Meijere) on the seed of Chamaecyparis lawsoniana Pari. imported from North America. The larvae of 

about 160 gall midge species develop on various species of 35 genera of broad-leaved trees in the 

world, producing various types of galls on terminal buds, stems, twigs, leaves, petioles, flowers, 

flower-stalks, fruits, and pods, or living under the bark, in decaying wood and bark, or as predators in 

the galls of mites or aphids. 

Most gall midges cannot be considered pests, but some of them may increase and then attain 

the status of pest. For example, in Central Europe, in Czechoslovakia, more than 500 gall midge 

species have been identified (Skuhrava 1987), 92 of which are associated with forest trees and may be 

considered as actual or potential pests. Thirteen species develop on coniferous trees and 79 develop 

on broad-leaved trees (Skuhrava 1983). At present, the following eight species of gall midges damage 

forest tree species and are actual pests: Contarinia fagi Rubsaamen on young trees of Fagus silvatica 

L, in forest nurseries or planted trees in submontane and montane areas; Contarinia querccina 

Rubsaamen on young oaks, Quercus robur L. and Q. petraea Liebl., in hilly country; Dasineura 

irregularis Bremi ( = Dasineura acercrispans [Kieffer]) on developing young leaves on terminal parts of 

the twigs of maple, Acer pseudoplatanus L., in lowlands and hilly countries; Harrisomyia vitrina Kieffer 

and Drisina glutinosa Giard. on leaves of young, medium-aged and old maple trees, Acer pseudoplatanus 

L., in submontane regions; Dasineura fraxinea Kieffer on leaves of young, medium-aged and old ashes, 

Fraxinus excelsior L, in hilly regions; Dasineura thomasiana Kieffer on leaf buds of young trees of Tilia 

platyphyllos Scop. and Tilia cordata Mill. in hilly areas; Dasineura kellneri Henschel ( = D. laricis F. 

Low) on buds of larch, Larix decidua Mill., in central and southwestern parts of Bohemia. 

The following 15 gall midge species represent potential pests of forest trees in Czechoslovakia: 

Thecodiplosis brachyntera Schwagr. and Contarinia Caeri Prell. on Pinus silvestris L and P. mugo Turra; 

Paradiplosis abietis Hubault on Abies alba Mill., Taxomyia taxi Inchbald on Tarus baccata L, 

Plemeliekla abietina Seitner on Picea excelsa Link., Resseliella piceae Seitner on Abies alba Mill., 

Contarinia marchali Kieffer on Fraxinus excelsior L., Mildola fagi Hartig on Fagus silvatica L, Dasineura 

fraxini Bremi on Fraxinus excelsior L, Zygiobia carpini F. Low on Carpinus betulus L, Didymomyia 

tiliacea Bremi on Tilia platyphyllos Scop. and Tilia cordata Mill., Dasineura tortilis Bremi on Alnus 

glutinosa Gaertn., Dasineura populeti Rubsaamen on Populus tremula L, Wachtliella rosarum Hardy on 

various species of Rosa, and Dasineura (Rhabdophaga, Helicomyia) saliciperda Dufour on various species 

of willows, Salix sp. The distribution areas of some of these gall midge species in the Palearctic 

Region were elaborated by Skuhrava (1987). 

Gall Midges as Members of Forest Ecosystems 

In relation to ecosystem studies, most gall midges may be considered part of the grazing food 

chain: the majority of gall midge larvae suck the sap of the plant tissues making or not making the 

galls. Another, but smaller part of the gall midge population belongs to the detritus food chain in 

which those species occur which suck sap from decaying or dead plant matter, i.e. the 

phytosaprophagous and mycophagous gall midges. Data about species composition, seasonal dynamics 

and function of gall midges in two types of forest ecosystems were obtained from studies organized 

within the International Biological Program on the Territory of Czechoslovakia. In 1973, stationary 

emergence traps were used to collect spiders, harvestmen, and insects, including Diptera, from the soil 

in a spruce monoculture at Kunicky, in the area of the Drahanska vrchovina Highlands, about 16°E 

and 4~N, at an elevation of 620 m a.s.l. The plant community was a type of unnatural woodland with 

unsuitable composition of Picea excelsa Link. The soils belong to the acid brown forest soil type 

(Vanhara 1983). In 1973, from the beginning of May up to the beginning of November, 1,108 

294 
specimens of adult gall midges emerged from soil under the tree traps. The majority of gall midges 

emerged in the spring. In terms of composition, most belonged to the zoophagous genera, 

Lestodiplosis (51 percent) and Trisopsis (11 percent). About 19 percent belonged to the 

phytosaprophagous species Porricondyla neglecta Mamaev. Strictly phytophagous gall midge species 

formed only 1 percent of the emerging specimens (Table 1 ). 

In 1971, 1972, and 1981, other ecosystem studies were carried out in a lowland forest of the 

Ulmeto-Fraxinetum-Carpineum type near Lednice na Morave using the sweep samples (Vanhara 1981, 

1986). In all, 7,815 specimens of Diptera were obtained in 1971, among them 3,417 specimens 

representing 711 species (9 percent) of gall midges. In lowland forest ecosystems, the family 

Cecidomyiidae is one of the richest families of Diptera. 

From late April to early October in 1981, 319 adult gall midges were collected. In lowland 

forests, the flight period of gall midges has two peaks, the vernal maximum in May and the autumnal 

one in early September. The species composition is more varied than that in the monoculture of Picea 

excelsa, with a predominance of the phytophagous species, Contllrinill tiliarum and Dasineura thomasillna 

(Table 2). 

Table 1. The composition of gall midge species emerging in 1973 from soil of 

a spruce monoculture (Picea excelsa Link.) at Kunicky in the 

Drahanska vysocina Highlands, Czechoslovakia, by means of stationary 

collecting emergence traps. 

Species or Number of individuals Percent Feedinf 

genus Males Females Adults of total habits 

Lestodiplosis 254 373 627 57 z 

Porricondyla neglects 80 126 206 18.5 PS 

Trisopsis 54 71 125 11 z 

Thecodiplosis brachyntera 2 4 6 0.5 p 

Kaltenbachiola strobi 2 3 5 0.5 p 

Cecidomyiidae, undetermined 46 93 139 12.5 

T o t a 1: 100 

1Abbreviations: Z - zoophagous, PS - phytosaprophagous, P - phytophagous. 

295 
Table 2. The gall midge species composition in the flood plain forest, 

Ulmeto-Fraxinetum-Carpineum type, near Lednice na Morave, 

Czechoslovakia, obtained by the sweeping method in 1981 

Species or Number of individuals Percent Feedinf 

genus Males Females Adults of total habits 

Contarinia tiliarum 30 46 76 24 p 

Porricondyla neglecta 19 40 59 18.5 PS 

Lestodiplosis 16 44 60 19 z 

Clinodiplosis cilicrus 13 30 43 13.5 PS 

Hycodiplosis 10 6 16 5 PS 

Dasineura thomasiana 3 8 11 3.4 p 

Macro lab is 4 7 11 3.4 PI 

Craneiobia corni 1 5 6 1.8 p 

Dasineura 6 6 1.8 PI 

Trisopsis 2 2 4 1.2 z 

Jaapiella 3 3 0.9 PI 

Lasioptera tiliarum 2 2 0.6 PI 

Didymomyia tiliacea 1 1 2 0.6 p 

Tricholoba 2 2 0.6 PI 

Aphidoletes aphidimyza 1 1 0.3 z 

Parallelodiplosis 

galliperda 1 1 0.3 PI 

Therodiplosis persicae 1 1 0.3 z 

Cecidomyiidae, undetermined 8 7 15 4.8 

T o t a 1 100 

1Abbreviations: P - phytophagous (gall-producing), PI phytophagous--

inquilines, PS =- phytosaprophagous, and Z - zoophagous 

LITERATURE CITED 

BARNES, H.F. 1951. Gall midges and economic importance. vol. 5. Trees. Crosby Lockwood & Son, 

London. 270 p. 

ISAEV, AS., BARANCHIKOV, Y.N., and MALUTINA, V.S. 1988. The larch gall midge in seed 

orchards of south Siberia, p. 29-43. In Berryman, AA, ed. Dynamics of Forest Insect 

Populations. Plenum, New York. 

SKUHRAVA, M. 1983. Gall midges (Cecidomyiidae, Diptera) of forest trees and their seeds in the 

Czech Socialistik Republik. Lesnictvi 29: 423-440. (In Czech, with English summary.) 

SKUHRA VA, M. 1986. Cecidomyiidae, p. 72-297. In Catalogue of Palearctic Diptera. Vol. 4. Budapest. 

441 p. 

SKUHRA VA, M. 1987a. Cecidomyiidae, p. 69-81. In Checklist of Czechoslovak Insects. II. Diptera. 

341 p. 

296 
SKUHRA VA, M. 1987b. Analysis of areas of distribution of some Palearctic gall midge species 

(Cecidomyiidae, Diptera). Cecidologia Intemationale 8: 1-48. 

SKUHRAVA, M., SKUHRAVY, V., and BREWER, J.W. 1984. Biology of gall midges, p. 169-222. In 

Ananthakrishan, T.N. Biology of Insect Galls. Oxford & ffiH. New Delhi, Bombay, Calcutta. 

362 p. 

STONE, A, et al., 1965. A catalogue of the Diptera of America North of Mexico. Washington, D.C., 

1696 p. 

VANHARA, J. 1981. Lowland forest Diptera (Brachycera: Cyclorrhapha). Acta Sc. Nat. Bmo 15: 1-32. 

VANHARA, J. 1983. Spruce monoculture Diptera (Brachycera: Cyclorrhapha). Acta Sc. Nat. Bmo 

17: 1-26. 

V ANHARA, J. 1986. Impact of man-made moisture changes of flood plain forest Diptera. Acta Sc. 

Nat. Brno 20: 1-35. 

297 
SEED GALLS OF SEMUDOBIA BETULAE 

(DIPTERA: CECIDOMYIIDAE) 

ON SPECIES OF BIRCH (BETULA SPP.) 

VACLA V SKUHRA VY 

Institute of Entomology 

Czechoslovak Academy of Sciences 

370 05 Ceske Budejovice, Czechoslovakia 

INTRODUCTION 

Semudobia betulae Winnertz, described in 1853, is the most common species of gall insect 

occurring on the genus Betula in the Palearctic and Nearctic regions of the world. S. betulae has been 

observed on four species of Betula according to Barnes (1951) and on 14 additional species according 

to Roskam (1977) . 

. At the Arboretum of Mlynany affiliated with the Institute of Dendrobiology of the Slovak 

Academy of Sciences, eight species of Betula from the Palearctic and Nearctic regions have been 

planted. Three of them are mentioned in the papers of Barnes and Roskam: B. pendula, B. ermanii, 

and B. papyrifera. 

In 1987 and 1988, the galls of S. betulae on the eight species of Betula were collected and their 

forms studied. Ten catkins were collected from each species and the number of attacked fruits 

recorded. 

RESULTS 

Normal seed of the birch consists of two parts: the middle part, i.e. the seed itself, and the 

large, round, rudimentary wings which assist in its dispersal. 

Gall form differed among various birch species. We found a great number of fruit having larvae 

or parasites inside the deformed seed gall and normal large seed wings. In some Betula species, on the 

other hand, the seed gall consists only of the middle part, without the wings. In other species, there 

are still other types of seed galls, which the wings are very small or only one part of the wing is 

developed. 

Normally developed galls were found only on B. ermanii, B. nigra, and B. pumilla. Great 

variability was found in B. pendula from Europe. The galls without wings were found on B. chinensis, 

B. microphylla, B. nigra, and B. papyrifera. Only B. maximowicziana was not infested. Since the fruit of 

this Betula species does not develop until 3 weeks after the flight period of S. betulae commences, its 

infestation is impossible. 

BARANCHIKOV, Y.N., MATfSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

298 
The results are summarized in the following table: 

Number of galls 

;Rer 10 catkins 

Betula species Distribution 1987 1988 

B. microphylla Bge. Middle Asia 8 12 

B. ermanii Cham. Northeastern Asia, Japan, Korea 16 7 

B. chinensis Maxim. Northern China, Japan, Korea 115 10 

B. pendula Roth. 

(-B. verrucosa) Europe, Asia 30 62 

B. maximowicziana Regel. Japan 

B. nigra L. Eastern U.S.A. 2 15 

B. pendula Roth. U.S.A. 115 19 

B. pumilla L. Northeastern U.S.A., Labrador 135 105 

B. papyrifera Marsh. North America 95 33 

The form of galls depends on the time when the first instar larvae start to develop in the fruit. 

Our data indicate that S. betulae are present on seven species occurring in the Palearctic and 

Nearctic regions. It appears that S. betulae can live on many species of the genus Betula in the 

northern hemisphere. It is interesting to note that the galls of S. betulae were also found on 

B. nana L in the Sumava Mountains of southern Bohemia, at an elevation of 1,000 m a.s.l. 

LITERATURE CITED 

BARNES, H.F. 1951. Gall midges of economic importance. vol. V. Trees. Crosby Lockwood and Son, 

London. 270 p. 

ROSKAM, J.C. 1977. Biosystemati~ of insects living in female birch catkins. 1. Gall midges of the 

genus Semudobia Kieffer (Diptera: Cecidomyiidae). Tijdschr. Entomol., 120: 153-197. 

299 
STRUCfURE, SPECIFICITY, AND EVOLUTION 

OF INSECT GUILDS RELATED TO CONES 

OF CONIFERS IN WESTERN EUROPE 

ALAIN ROQUES 

Institut National de Ia Recherche Agronomique, INRA-CRF-Station de 

Zoologie Forestiere, Ardon 45160, Olivet, France 

INTRODUCTION 

Patchy and ephemeral resources, such as the cones of conifers, can be very useful in the study of 

plant-insect relationships. Studies of such relationships in forest entomology are typically complicated 

by the spatial and temporal characteristics of the host plants, which occur over vast areas and have 

lifespans of decades or even centuries. The reproductive structures of conifers, on the other hand, are 

much more easily studied because they mature within 1 to a few years and occur as discrete, easily 

sampled units. They also play a unique role in forest ecosystems. 

Seed cones, which correspond to female flowers in most gymnosperms (Pinaceae, Taxodiaceae, 

Araucariaceae, most Cupressaceae), develop both as singular units and as integral parts of cone-bearing 

trees. Though development varies with tree species, general trends appear similar, corresponding to 

the progressive development of the female flower into a lignified cone that can release mature seeds. 

These overall similarities in cone development among most conifers facilitate a comparison of the 

fauna inhabiting cones (Roques 1988a ). 

Cone maturation is always extremely rapid compared to tree lifespan. The morphological, 

physiological, and biochemical changes which occur during the lifetime of the reproductive structures 

are thus condensed into a much more limited time and space (cone size varies from 0.6 em in 

Juniperus sabina to 15 em in Abies alba, and time from flowering to seed release ranges from 

6-1/2 months in Larix decidua to 2-1/2 years in Pinus silvestris, for instance). Very distinct 

environmental conditions are thus offered to insects during successive and temporally restricted periods. 

Moreover, in most conifers spatial distribution of cones is heterogeneous among trees as well as within 

trees (Mattson 1979) and cone crop appears to vary over time, generally being neither annual nor 

cyclic (masting phenomena, according to Fenner 1985). 

Individual cones may therefore be viewed as temporary subunits of the forest biocenosis which 

form discrete habitats with a limited carrying capacity for possible inhabitants. Niche characteristics, 

especially size limitations, would predict a highly specific entomofauna adapted to host discontinuity in 

space and time. 

Though a large body of literature has dealt with the functioning of insect guilds of similar 

structures of angiosperms (among many others, Janzen 1969, 1970, Zwolfer 1979, 1982, 1987, 1988), 

very few studies have provided a synthesis of the relationships between cones and associated insect 

guilds, with the exception of some notable work done in eastern Europe (Stadnitskii 1971, Stadnitskii 

et al. 1978, Skrzypczynska 1977, 1981, 1982, among others). In this contribution, which is part of a 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

300 
wider study of cone-insect relationships (Roques 1988a), I synthesized the European literature with the 

following goals: 1) analysis of the structure of ecological groups in cones of native and introduced 

conifer species in western Europe, 2) specificity of the host of individual cone-insect relationships, and 

3) exploration of the consequences for the structure and evolution of insect guilds. 

ECOLOGICAL GROUPS RELATED TO CONES: DIVERSITY AND LIMITATION 

Insects inhabiting cones in western Europe can be divided into three ecological groups in 

relation to trophic habits: a) phytophagous insects with their parasite and predator complexes, 

b) mycophagous and detritivore species developing in the detritus food chain deriving from the 

previous group, with their own natural enemies, and c) insects using the galleries made by phytophages 

as hibernating shelter sites. This structure of entomological communities is, naturally, based upon the 

phytophagous group, whose previous damage creates conditions that support development of the other 

groups. 

Insects Using Cones as Hibernating Sites 

These species are uncommon. Only a few species with no accurately defined tropic relation, are 

regularly encountered overwintering within cones: adults of Rhizobius chrysomeloides Hbst. (Coleoptera: 

Coccinellidae) and some stages of Leptothorax affinis L (Hymenoptera: Formicidae) in P. silvestris 

(Roques 1977); some stages of Crematogaster spp. (Hymenoptera: Formicidae) in Mediterranean pines; 

adults and nymphs of Gastrodes abietum Bergroth and G. grossipes De Geer (Hemiptera: Lygaeidae) in 

spruce (Roques 1983). These insects will be excluded from the following discussion. 

Mycophagous and Detritivore Species 

Larvae of several species commonly develop on fungi and detritus in cone galleries made by 

phytophages. Dipterous larvae are exclusively observed in western Europe: Chloropidae, one species, 

and Cecidomyiidae, one species. These larvae do not directly attack cone structures but may, as does 

Camptomyia pinicolana Mam. (Cecidomyiidae), seed browning that leads to seed abortion (Roques 

1983). The detritivore subguild is more important in other European regions. In addition, 15 other 

species, mainly Diptera but also Coleoptera (Cryptophagidae, Anobiidae, Lathridiidae) have been noted 

in Poland and in the European part of the Soviet Union (Skrzypczynska 1977, 1981, 1982, Stadnitskii 

et al. 1978). 

Phytophagous Species 

By contrast, diversity in families and orders is a dominant feature of the phytophagous group. 

Larvae of weevils, microlepidoptera, gall-midges, and seed-chalcids, among others belonging to 13 

families and four orders of insects are known to feed on cones of the various conifers growing in 

western Europe (Fig. 1a, from data in Roques 1983). In addition, mites of the family Eryiophiidae 

have been reported, e.g. Trisetacus spp. (Roques 1983, Roques et al. 1984). 

This diversity, however, is only superficial. The number of species and, more importantly, the 

number of genera observed in the cones are limited. Fifty-nine species from only 30 genera are 

currently recorded in western Europe (Fig. 1b, from Roques 1983, Roques et al. 1984, Roques and 

Raimbault 1986). The subsequent total of recorded phytophages and detritivores is 61 species and 32 

genera. The same values total only 72 and 33, respectively, when all of Europe, including the 

European part of the Soviet Union, is considered (calculations from data in Annila 1976, Wiersma 

1978, Skrzypczynska 1977, 1981, 1982, Stadnitskii et al. 1974, 1978). This shows both relative stability 

301 
FREQUENCY 

NUMBER 

OF SPECIES 

20 

,0 

3 

D 

NUMBER OF 

SPECIES 

10 

B 

~ LEPIDOPTERA 

c::J HYMENOPTERA 

~DIPTERA 

-COLEOPTERA 

I!IliDl ACARINA 

.. .. 

I 

6 8 NUMBER OF SPECIES I GENUS 

FREOtJENCY 

Ill CONOXENlC SPECIES 

m CONOPBll.JC SPECIES 

~ EtJRYTROPIDC SPECIES 

~ LEPIDOPTERA 

c:J HYMENOPTERA 

~ DIPTERA 

IB COLEOPTERA 

I!IIIJll ACARINA 

FAMILIES 

NUMBER OF PARASITES 

PER PBYTOPBAGOtJS SPECIES 

Figure 1. Faunal characteristics of insect guilds related to cones in western 

Europe: a) families and orders involved in phytophagous and detritivore 

species (* 1 detritivore species), b) extent of speciation within phytophagous 

genera(* 2 genera with 1 detritivore species), c) frequency of entomophagous 

species per phytophagous species, and d) specificity to cones and 

developmental features shown by the phytophagous and detritivore species. 

302 
in cone-insect relationships at the continental level and the present limitation of speciation processes 

within cones to a reduced number of genera, whose species are specializing in the exploitation of these 

distinct substrates (especially Anthomyiids of the genus Strobilomyia, Chalcids of the genus Megastigmus, 

Pyralids of the genus Dioryctria, and Anobiids of the genus Emobius). 

The guilds of phytophagous insects associated with cones include three trophic strategies by 

which the resource is partitioned. A first group, representing 40 percent of the insects (27 /59), feeds 

on cone tissues as well as on seeds: conoseminiphagous insects, e.g. members of the Anthomyiid genus 

Strobilomyia, members of the tortricid genera &rbara, Petrova, Cydia, and Pammene, and the weevil 

Pissodes validirostris, among others. The second group, less important (19/59), develops only on cone 

tissues: conophagous insects, e.g. some members of the Pyralid genus Dioryctria and Argyresthiidae of 

the genus Blastotere). The third group (15/59) is specialized in seed exploitation: seminiphagous 

insects, e.g. members of the chalcid genera Megastigmus and Torymus and members of the Cecidomyiid 

genera Plemeliella and Resseliella, among others. It must be noted that all the insect species from a 

single genus exploit the same cone level, independently of tree species. These characteristics of the 

phytophagous group--diversity of families and limited speciation process related to a similar 

specialization in resource exploitation by species of the same genus--may be viewed as the result of an 

evolutionary process leading to complete utilization of the niche. 

Parasite and Predator Complexes 

Only 38 of the 61 phytophagous and detritivore species are presently known to have parasites 

and predators within cones in western Europe (data compiled by Roques in Yates 1988). One hundred 

twenty-two species, mainly Hymenoptera, have been identified in this group (Table 1 ). 

The number of parasite species per host species is limited, generally fewer than 10 (Fig. 1c). It 

has been assumed that the cryptic nature of most cone insects underlies this phenomenon (Yates 1986). 

Thus the number of natural enemies observed in phytophagous insects that can feed on structures 

other than cones is strongly affected by the type of tissue occupied, e.g. three parasites in cones versus 

20 in shoots for the pine shoot moth, Rhyacionia buoliana Schiff., in the same French localities 

(Roques 1977). 

DEGREE OF SPECIFICITY OF THE V ARlO US INSECT GROUPS 

High Host Specificity for Most Phytophagous Insects 

Seventy-one percent of these species, defined as stenoconobiont species (after Stadnitskii 1971), 

need to complete their larval development, at least in part, within cones (Fig. 1d, from Roques 1988a). 

More than half--the conophilic show an extreme adaptation in spending their entire larval and pupal 

development within cones species as opposed to the conoxenic species, which exit the cone to pupate--

(Fig. 1d). All seminiphagous species exhibit this former type of development. Close adaptation to 

seed substrate thus appears as the result of an extreme niche specialization. 

Conversely, less than one third of common phytophages, the heteroconobiont species, are able to 

develop in other tree structures, such as buds and shoots. Most of them (14/19) damage the cones 

only occasionally, when insect population density is out of proportion to the resources offered by the 

normal host, e.g. as in outbreaks of the larch bud moth, Zeiraphera diniana Guenee (Roques 1988b ), 

and as with pine shoot moths, Rhyacionia pinicolana Dbld. and Rh. buoliana Schiff., in young stands 

(Roques 1977). A minority of heteroconobiont species do prefer the cones and feed occasionally on 

other vegetal structures. Dioryctria mutatella Fuchs may develop in pine shoots in case of cone crop 

303 
Table 1. Parasites and predators associated with phytophagous cone insects in 

western Europe 

Order Family Number of species 

Hymenoptera Ichneumonidae 43 

Braconidae 28 

Pteromalidae 22 

Torymidae 5 

Eulophidae 4 

Eupelmidae 3 

Tetrastichidae 2 

Platygasteridae 1 

Eurytomidae 1 

Encyrtidae 1 

Trichogrammatidae 1 

Cynipidae 1 

Diptera Tachinidae 5 

Lonchaeidae (predator) 2 

Neuroptera Chrysopidae (predator) 1 

Rhaphidiidae (predator) 2 

failure (Charles and Roques 1977). This certainly confers an adaptive advantage upon these latter 

species, allowing their populations to minimize the consequences of irregular cone crops. 

Despite appearances, however, no European cone and seed insect species is entirely host-specific. 

The apparent specificity observed in western Europe results from the present range of conifers in this 

geographical region, where in several cases only one species per genus survived after Quaternary 

glaciations, e.g. Larix, Picea, and Abies. 

The example of the Megastigmus species is significant. The speciation process is highly 

developed in this genus as compared with other cone insects, resulting in seven native species, to 

which, subsequently, four species introduced from North America have been added (Roques 1983). 

Larvae of these chalcids developing entirely in seeds are completely at the mercy of host selection 

pressure, with no possibility of escape (Labeyrie 1977). Therefore, conifer taxa may be assumed to 

serve as platforms for adaptive radiation of Megastigmus, insect species ultimately mirroring conifer 

speciation. Such a process is observed, but with a substantial evolutionary lag. Native conifer species 

in western Europe are each attacked by a single Megastigmus species, with the exception of Pinus spp., 

in relation to which disappearance with glaciations probably explains the absence of chalcids (Roques 

1988a). However, where sympatric stands of congeneric host species exist, e.g. Juniperus spp. in central 

and mediterranean France, they are colonized by the same chalcid species (Roques et al. 1984). In 

addition, records in arboreta where exotic and native tree species are mixed show that each 

Megastigmus species is still capable of attacking allopatric Eurasian congeners of the natural host 

(Table 2), whereas these allopatric species are colonized by other chalcid species in their native areas. 

Similar results have been obtained with most other cone insects, e.g. Strobilomyia spp. and Cydia spp. 

(Roques 1983). Host specificity thus remains at a superspecific level, though local adaptive differences 

in insect populations probably exist. 

304 
Table 2. Host range of Megastigmus species observed within seeds of native 

and exotic species growing at the Arboretum des Barres (France) 

MEGAS11GMUS 

SPECIES 

M.suspectus • • • • • • 

M.suscectus var. 

pinsapinis • • • • • • 

M.pic:us • • 

M.stroci lobi us • • • 

M.pinus• • 

M.spermotrcphus • • • 

* Insect species introduced along with host species 

**Introduced host species 

High Phenological Synchrony with Cones 

There is close phenological coincidence of attack period in phytophagous insects with the 

appearance of unique, ephemeral stages in cone development. This is observed in all conifer species 

(Roques 1983, Roques et al. 1984). Most phytophagous insects are univoltine species, apart from some 

Dioryctria spp. (Roques 1983), and close synchrony in attack period is probably an adaptation to 

structural changes occurring within the cone which differentiate it from other tree structures, especially 

buds and shoots. 

Fig. 2, based on the homology in cone development observed in western conifers, presents a 

synthesis of colonization of successive cone development phases by the 59 European phytophages. The 

stenoconobiont core of cone entomofauna is essentially recruited during cone growth and onset of seed 

development, when physical and chemical changes are both more substantial and more rapid. By 

contrast, previous and subsequent development phases, during which cones may be less distinct from 

surrounding tree structures, are dominated by heteroconobiont species. 

Fig. 2 also shows the decrease in conoxenic species, due to successive departures from the cone, 

after the completion of cone growth. This may be considered an "evasion" strategy (sensu Zwolfer 

1982), minimizing intra- and interspecific competition for limited cone resources. 

305 
NUMBER OF INSECT 

SPECIES OBSERVED 

NUMBER OF INSECT 

SPECIES 

INSECT ATTACK 

INSECT ATTACK 

CONEPBASE I II ~ .c ~ 

~ ... 

~ 5 

s:Q E B 

'B t!) g. 

s:Q ~ ~ 'i s.. 6 6 ~ "" ~ 

~ u u Q 

0 ~ ~ -g -

~ ·~ 0 

til ~ 

a:: f.l) 

.... 

0 

... 

~ 

8 

DEVELOPMENT 

WITHIN CONE 

·~ 

:.:3 

[ZJ EURYTROPIDC l HETEROCONOBIONT 

W SPECIES PHYTOTROPIDC 

- CONOXENIC l STENOCONOBIONT 

f.·.;.;~ CONOPmLIC SPECIES 

!.•,•.•.! CONOPHAGES 

~ CONOSEMINIPHAGES 

~~~ SEMINIPHAGES 

Figure 2. Patterns of cone colonization by the phytophagous and detritivore 

guilds during cone development as a function of a) host specificity and 

b) trophic level. Calculations based on the 61 species commonly observed in 

cones in western Europe. 

306 
Comparative Polyphagy of Etomophages and Phytophages 

In P. silvestris, for instance, 14 of the 15 entomophages, whose cone insect host is identified, 

also prey on insects from other structures of scots pines (trunk, shoots, buds) or insects developing in 

the cones of other tree species (Roques 1988a ). Similar relationships have been established in larch 

(Roques 1988b) and spruce (Stadnitskii 1971). More generally, at least 80 of the 122 entomophages 

(i.e. 66 percent) recorded in cones in western Europe show alternate hosts that do not develop in 

cones. Only a few chalcids of the genera Mesopolobus, Anogmus, Amblymerus (Pteromalidae), Eupelmus 

(Eupelmidae ), and Torymus (Torymidae) seem specialized for the attack of seminiphagous insects. 

Polyphagy of entomophages effectively decreases from conophagous to seed insects, in relation to the 

increasing specialization of hosts (Roques 1988a ). 

The parasite speciation process in adaptation to phytophagous hosts thus appears to be more 

delayed than phytophage adaptation to conifers. Several factors may be involved. Differences in 

parasite complexes in regard to the plant substrate have previously been noted in heteroconobiont 

species. A substantial similarity is also observed in some phytophagous species of the same genus 

colonizing various tree structures, e.g. Pissodes spp. (Mills and Fisher 1986). It can be assumed that 

the parasite complex evolved from preadapted entomophages of these other insects. The slow progress 

of this process can be inferred from the variations in parasitism rate observed when a phytophagous 

cone insect colonizes a new introduced host. P. validirostris Gyll. immediately adapted to cones of 

Pinus contorta when this tree species was introduced into Europe. However, Pissodes parasites 

apparently faced barriers in locating their normal host in an introduced conifer. Parasitism levels 

remain low in P. contorta (2 percent versus 40 percent in P. silvestris) in Finland (Annila 1976) as well 

as in France (Delplanque et al. 1988). Parasite colonization thus apparently requires adaptation to 

both phytophagous host and cone host. 

CONSEQUENCES FOR GUILD STRUCIURE AND EVOLUTION 

Analogies in Cone Phytophage Succession in Native Tree Species 

Similar specializations in cone resources are shown by congeneric insect species with respect to 

the synchrony of insect attack period with cone development; this results in a relative similarity of 

faunal structure within each native conifer species. Three main groups, within which fauna are 

homologous, are clearly distinguishable (Fig. 3). 

Pinaceae with annual seed-cone development (i.e. Picea abies, L. decidua, A alba) show quite 

homothetic fauna where distinct insect species from the same families (and often from the same genus) 

colonize the same cone development stages in four successive attack periods. 

Although tree species fauna also appear homologous, insect families and genera colonizing 

Juniperaceae are quite different from the previous ones. In addition, sympatric Juniperus spp. 

(l communis and l nana in northern areas versus l oxycedrus and l phoenicea in mediterranean areas) 

have common fauna. The peculiar case of L thurifera will be considered further on. 

Pinaceae with superannual seed-cone development (i.e. Pinus spp.) have comparatively fewer 

cone phytophages and their fauna are more dissimilar. Three subgroups can be delimited: pine 

species of the silvestris group (P. silvestris, P. nigra, P. uncinata, P. mugo), mediterranean pines 

(P. pinea, P. pinaster, P. halepensis), and P. cembra (subgenus strobus). The single common component 

among these species is the occurrence of Dioryctria spp. (Pyralidae) and, in the two former groups, the 

weevil, Pissodes validirostris. The latter tree species is colonized only by three nonspecialized insects. 

307 
PHASE. 

II 

Ill 

IV 

FEMALE BUD BURS'l' 

(annual cycle) 

OR 

ONSET OF CONE 

DEVELOPMENT 

IN THE Znd YEAR 

(superannual cycle) 

RAPID· 

GROWTH 

SLOW 

GROWTH 

LIGNIFICATION 

GROUP I GROUPll 

IORTRICIDAE 

GEOMETRIDAE 

ANOBIIOAE 

PYRALIOAE 

GROUPW 

PYRALIDA£ 

TORTRICIDA£0 

PYRALIOAE 

~ 

~ STENOCONOBIONT 

SPEClliS 

r-1 HETEROCONOBIONT 

L__.1 SPEcms 

Figure 3. Classification of conifer species native in western Europe as a 

function of homologies seen in successive attacks of insect and mite families 

during cone development. Group I: Pinaceae with annual seed-cone development; 

Group II: Juniperaceae; Group III: Pinaceae with superannual seed-cone 

development. 

The magnitude of the differences between groups with respect to the structural regularity within 

each group suggests a common origin for the fauna occupying cones of conifer species from groups 

with similar reproductive cycles. The insect fauna occurring at present may be the result of a further 

parallel diversification within each group. 

Variation in Phytophage Guild with Tree Species and Stands 

The total number of phytophagous species recorded in western Europe (species richness) varies 

with tree species, irrespective of cone size (Fig. 4a). However, an analysis of the respective 

contributions of stenoconobiont and heteroconobiont insects to species richness leads me to group tree 

species in a way similar to that above (Fig. 4b). 

This confirms the existence of similarities or links in the colonization process within each of 

these groups. Pinaceae other than Pinus spp. show the largest diversity in cone insects, including a 

majority of stenoconobiont species. Juniperaceae have fewer species, but all are specialized in cones. 

Mediterranean pines and pines of the silvestris section are clearly separated, specific characteristics of 

the former being close to Juniperaceae. Fauna of the latter subgroup, though more diverse, is less 

closely adapted (50 percent of heteroconobiont species). Last of all, Pinus cembra appears similar to 

most introduced species: it is characterized by very low colonization, mainly by heteroconobiont 

species. 

308 
SPECIES 

RICHNESS 

15 

10 

0 

Larix decidua 

Pinus silvestris 

Pse~dotsuga mensiezii* 

Pinus nigra Juniperus phoenicea ___ ...,_ __ _ 

Juniperus oxycedrus Pinus uncmata Pinus h·alepensis 

Cedrus atlantica* 

Cupreuus aempervirens* __.__ 

Picea abies 

Abies alba 

JunipcruJ communis Juniperus ttlurifera Pinus pineae Pinus pinaster 

~ 

Pinus contort"ft Pinus c•mbra 

Juniperus sabina 

.... 

a 

10 15 CONE LENGTH (em) 

Figure 4. Species richness in phytophagous guilds related to cones in western 

Europe: a) relation with cone length and b) respective contribution of 

stenoconobiont vs. heteroconobiont species. *Introduced conifer species. 

However, species richness provides a biased view of relationships between tree species and insect 

guilds by hiding possible variation with geographical range. When species packing (i.e. the number of 

species recorded in a given stand under standard sample collections) is the measure used, such 

variation appears in most conifers (Fig. 5). 

Interspecific variation within a given area does not seem significantly related to the date of first 

reappearance of tree species after Quaternary glaciations, at least in French regions where sufficient 

paleobotanical data are available (Roques 1988a). 

Conversely, intraspecific variation within tree ranges appears related to species reappearance in a 

species like Picea abies, which has a continuous distribution (Fig. 6). Species packing varies along a 

gradient following the postglaciation development of spruce from eastern Europe. The relative 

importance of closely adapted insects decreases from the location of the secondary evolution center of 

P. abies; ZwOifer (1987) noticed a similar pattern in thistle-head phytophagous guilds. The asymptotic 

curve indicates that insect evolutionary delay is limited in regard to host range expansion. When this 

progress is continuous, the faunal composition, including very specialized seed insects, can occur in less 

than 2,000 years. This development lasts longer in isolated stands of human creation, such as in the 

Pyrenees (Fig. 6). First colonization is, nevertheless, carried out by a certain number of insect species 

that are cone-specialized without being tree-specific. Faunal recruitment consequently results from 

309 
NUMBER OF 

HETEROCONOBIONT 

SPECIES 7 

8 

4 

3 

2 

0 

Paeudoaug.. 

menziaii 

Plnuapin.ster 

Pinw pine• ..,..._. 8Bmp11Mrirerw 

• 

Pice. abi• 

Group~ ) 

1..8rix decidua 

Jc Juniperw c:arnnan. , 

Jt .Nnipena ltu'ifcr8 

Js JIMlipena ubine 

::~:;~· AI::-.:~~ 

Js Group II Juniperw axycearw 

Jc Jt Juni..,. phaenicea 

2 3 4 56 7 8 9 NUMBER OF 

STENOCONOBIONT SPECIES 

Figure 5. Variations in species packing of phytophagous guilds observed 

within cones through the natural range of four conifer species. Species 

packing is indicated by numbers within circles, host range by either hatching 

or points. 

development of preadapted insects in cones of native conifer species. Early occurrence of insect 

species more adapted to tree species may be explained by insect flight capacity relative to stand 

isolation, ornamental trees being "relays" for the spread of insects, as shown for Douglas-fir (Roques 

1986) and mediterranean cypress (Roques and Raimbault 1986). 

Observations in species showing a relictual natural range following Quaternary glaciations 

confirm these results. In J. thurifera and P. cembra, cone fauna probably disappeared partially or 

completely during that period. Fig. 7 presents their respective recolonization patterns (from data in 

Roques 1983, Roques et al. 1984). In J. thurifera, differences among species result from local 

recruitment of insects occupying similar cone structures in either northern or mediterranean junipers, 

depending on stand location. In P. cembra, the recolonization progresses from insects observed on 

other sympatric conifers of genera Pinus and Picea, one of them, Cecidomyia pini, feeding on other 

structures than cone (i.e. foliage) in the usual host. Nevertheless, this last process has barely begun, 

no conoseminiphagous or seminiphagous (i.e. specialized) insects having been observed. 

In introduced tree species, relative taxonomic isolation--number of congeneric species in the area 

of introduction (ZwOifer 1982)--also plays a decisive role in the rapidity of insect colonization. Exotic 

species without native European congeners (e.g. Pseudotsuga, Tsuga, Sequoia, Cryptomeria, 

Chamaecyparis, and others), or even without taxonomically close species in the same genus in some 

cases (pines of the strobus section), generally show a majority of conophagous insects (Roques 1983, 

1988a ). The conoseminiphagous minority is observed to include heteroconobiont or ubiquitous 

stenoconobiont species related to the insect genera commonly found in cones in the tree's native area. 

No seminiphagous insects are noted, except when Megastigmus chalcids have been introduced along 

with the host. Conversely, the phytophagous guild is much more complete in Pinus contorta or Asian 

spruce species: specialized insects passing to these new hosts from taxonomically close European pines 

of the silvestris section and from Norway spruce, respectively (Roques 1983 1988a ). 

310 
NUMBER 

OF SPECIES 

20 

10 

7 ••••• ••••••••• 

..-a ~~-7-a 

"' SPECIES PACKING 

+ STENOCONOBIONT SPECIES 

.4.3 -----·2~---------·1 ____ ., 

•• • .l _______ 2 ____ ___....----

DATE OF 1st APPEARANCE 

DURING THE QUATERNARY 

~---~------------------~---------------------.-~--~ 

Figure 6. Relationships of species packing and host specificity in the 

phytophage guild of cones of Picea abies with the date of reappearance of this 

tree species during the Quaternary era in several regions of Europe: 

1) Polish Carpathians (from Skrzypczynska 1982), 2) Upper Adige (from Del 

Favero and Masutti 1974), 3) Maurienne Valley, 4) Brian~onnais, 5) Vosges; 

6) southwestern France, 7) western Pyrenees, and 8) Fontainebleau Forest (from 

Roques 1983). 

CONCLUDING REMARKS 

The structure and composition of the phytophagous cone and seed insect guilds, the most 

characteristic among cone insects in western Europe, thus appear to result from an adaptive process 

which began largely before the Quaternary era. I have previously discussed the assumption of a 

common original fauna colonizing the new cone niche based on its presumed appearance during the 

lower Carboniferous period in conifer ancestors, the Cordaitales, from nonspecialized insects feeding on 

other tree structures (Roques 1988a ). Though this idea remains highly questionable, the present results 

clearly suggest a common colonization during the Tertiary era, at least in Pinaceae and Juniperaceae. 

From these fauna three distinct patterns of phytophagous guilds would have evolved through adaptation 

to the different length of vegetative reproductive cycle, followed by parallel diversification in regard to 

increasing cone specialization. It must be noted, however, that the current situation may be 

substantially distorted because it results from an evolutionary process that involved many conifer 

species and genera that are now extinct in Europe--10,000 gymnosperm species existing in the 

Cretaceous period as opposed to the 600 existing today, according to Wieland (in Gaussen 1955). 

From this point of view, the present heteroconobiont species may be considered precursors of 

future new stenoconobiont species, but the large dominance of this latter group in phytophagous guilds 

also indicates that the niche may be full in native tree species. The current range of host acceptance 

in stenoconobiont species shows, however, the probable direction of the actual evolution of 

phytophages related to cones: new species diversification through adaptation to a single host in 

response to relative geographic isolation in many conifers in western Europe. 

Evident similarities in structure and functioning are noticeable when one compares cone insect 

guilds to those of other habitats characterized by limitation in space and time, especially the 

thistle-heads, as described by ZwOlfer (1979, 1982, 1987, 1988). In the two cases, insect specialization 

311 
.-· ·-··-··-··"'· 

Figure 7. Recruitment of new cone phytophages in certain parts of the range 

of Pinus cembra and Juniperus thurifera from preadapted fauna of related 

sympatric conifer species. 

is directly associated with the occurrence of evasion strategies minimizing competition for limited food 

resources. Thus cone-insect systems are similarly observed to include partitioning of cone space, both 

by insect specialization in specific cone structures and by limitation in the number of competitors for 

the same structure, and sharing of time by adaptive differentiation of both arrival and exit of insect 

species (Rappaport and Volney 1986). However, this system faces an additional limit in food resources 

imposed by annual crop fluctuations, which do not occur to this extent in other systems. The latter 

evasion strategies are ineffectual when cones do not exist over large areas. 

Other adaptive mechanisms, especially prolonged diapause, have been shown to allow the 

survival of insect species depending on cone occurrence (Bakke 1963). It is particularly interesting to 

note that prolonged diapause is not only limited to stenoconobiont species (at least 55 percent show it, 

312 
to our present knowledge), but this phenomenon is also more effective in insect species attacking 

conifers with an annual seed-cone development (Roques 1989). This confirms the existence of previous 

differences in faunal evolution pattern. Prolonged diapause is also a general characteristic of 

seminiphagous insects, emphasizing the occurrence of seed-insects as "indicators" of the current status 

of phytophage guild specialization in each tree species. 

Particular relationships between the cones and the remaining forest biocenosis are initiated by 

the consequences of the following factors: insect evolutionary delay in regard to conifer speciation and 

occurrence of heteroconobiont species and dominant polyphagy in entomophages. Cones, then, 

constitute a nutritional reservoir for insects damaging other tree structures as well as corresponding to 

a potential reservoir of alternate hosts for parasites and predators commonly found in the biocenosis. 

Cones also develop in competition with other vegetal structures for the consumption of photosynthesis 

products (Kozlowski 1971 ). These interrelations imply that no intrinsic regulation can exist at 

quantitative levels in cone-insect systems considered separately from the biocenosis, though the 

qualitative composition of cone entomofauna depends mainly on cone development. The definition of 

merocenosis, as used by Balogh (1958), has previously been proposed to qualify such a functioning in 

the case of Pinus silvestris (Roques 1977). Concordant data recorded in other species (Roques 1988a) 

suggest that the notion of merocenosis can be generalized to insect guilds related to cones in each 

native conifer. 

SUMMARY 

Cones can be regarded as dynamic plant microunits, with both limited lifespan and size and 

highly variable spatial and temporal distribution. Fifty-nine phytophages, two detritivores, and 122 

entomophages have been regularly observed to develop within cones in western Europe. Entomofauna 

structure in native conifer species is characterized essentially by phytophagous guilds highly specialized 

in cone utilization, the other insect groups being mainly polyphagous. However, specialization shown 

by most phytophages appears delayed in regard to the evolution of conifers, each insect species being 

still capable of attacking cones of congeneric tree species. Possible origin, evolution, and direction of 

future diversification of fauna in further adaptation to hosts are discussed. Finally, entomofauna 

related to each conifer species is defined as a merocenosis, whose regulation is under the control of 

forest biocenosis. 

ACKNOWLEDGEMENTS 

I am very much indebted to Dr. N.G. Rappaport, USDA Forest Service, Pacific Southwest 

Forest and Range Experiment Station, Berkeley, for help in reviewing the manuscript and to 

Mr. J.P. Raimbault, INRA Orleans, for technical assistance. 

LITERATURE CITED 

ANNILA, E. 1976. Cone and seed insects problems in seed orchards in Europe, p. 369-380. 

14th IUFRO World Congress, Oslo. 

BAKKE, A 1963. Studies in spruce cone insects, Laspeyresia strobilella (L) (Lepidoptera: Tortricidae ), 

Kaltenbachiola strobi (Winn.) (Diptera: Itonidae ), and their parasites (Hymenoptera) in Norway. 

Skogforsoksv. 19: 1-151. 

BALOGH, J. 1958. Lebensgemeinschaften der Landtiere. Akad. Verlag, Berlin. 560 p. 

CHARLES, P.-J. and ROQUES, A 1977. Observations sur Ia biologie de DioryctriLl mutate/fa Fuchs 

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Working Party Conf., IUFRO, Brian~on. INRA, Versailles. 

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France par le chalcidien ravageur, Megastigmus spermotrophus Wachtl. (Hym.: Torymidae), 

p. 685-694. 18th IUFRO World Congress, Ljubljana. 

ROQUES, A 1988a. La specificite des relations entre cOnes de coniteres et insectes infeodes en 

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ROQUES, A 1989. New results and some thinkings about significance and induction of prolonged 

diapause in cone insects with particular references to the larch cone fly (Lasiomma melania) and 

314 
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33: 103-122. 

315 
SEED PRODUCfiON AND CONE-FEEDING 

INSECfS OF PINUS PUMILA 

ON THE KAMTCHATKA PENINSULA: 

ASPECfS OF COEXISTENCE 

PETR A KHOMENTOVSKY and L.S. EFREMOVA 

Kamtchatka Department of the Environment 

Far-Eastern Branch of the U.S.S.R. Academy of Sciences 

Prospect Rybakov, 19-A 

Petropavlovsk-Kamtchatky 683024 U.S.S.R. 

Kamtchatka Forest Experiment Station 

Far-Eastern Research Institute of Forestry 

Kluchevskaya str., 24-2 

Petropavlovsk-Kamtchatsky 683002 U.S.S.R. 

INTRODUCTION 

Insects attacking seeds and cones of trees are significant for their economic consequences as well 

as for the ecological role in vegetation dynamics. Currently much is known about seed and cone 

insects feeding on upright trees (see Roques, this volume), but almost nothing is known about cone 

inhabitants of prostrate pines Pinus pumila (Pall.) Rgl., P. albicaulis Engelm., P. mugo Tur. These 

three vicariant species from young mountain systems of the northern hemisphere have evolved in 

unfavorable environments which have favored peculiar patterns of seed production and insect-host 

relations. Cone insect populations are strictly determined by well known periodicity of seed production 

which often causes the evolution of diapause in cone-feeding insects. This phenomenon occurs in 

upright trees and is perfectly illustrated by Lasiomma melania on Larix kamtchatica on the Kamtchatka 

Peninsula. Unlike Larix, Pinus pumila, whose seeds develop over 2 years, has peak crops every 2 to 3 

years but in fact produces some cones every year. This happens because seeds are produced on 

mosaically dispersed local patches of trees varying in micro-climate and other environmental factors. 

There are small, contiguous patches of good seed production in almost each region. Another 

important feature of the stochasticity of seed production is that seed dispersal is affected by the 

nutcracker, Nucifraga caryocatactes L., which leads to wide exchange of genetic material, and, 

consequently, to high ecological valency of the tree species. In sharp contrast to the typical strong 

antibiosis towards xylophagous insects: the trees apparently tolerate parasitic-commensal relationships 

with the seed and cone feeding species. 

On the other hand, the plant is highly vulnerable to the attack of highly specialized insects. 

Pinus pumila cones, growing on the Kamtchatka Peninsula, are damaged by only two insect species--

Cecidomyia pumila Mamaev et Efremova sp.n. (Diptera: Cecidomyiidae) and Eupithecia abietaria Goeze 

(Lepidoptera: Geometridae ). 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

316 
Seed Yields of Pinus pumila 

Pinus pumila on the Kamtchatka Peninsula produces seeds along the whole altitudinal profile of 

its range, from the sea coast almost up to the timber-line (about 1350 to 1400 m. above sea level). It 

can occur practically in all sites (Fig. 1 ), if not overs haded for more than 50 percent. 

Cone size (length and diameter) declines with increasing altitude more definitely than their mass 

(correspondingly r.l = -0.73; r.d. = -0.79; r.m. = -0.41). Cumulative seed quantity increases very 

definitely with altitude (r = 0.76), mainly owing to increasing numbers of imperfect seeds. Seed output 

per cone (seed mass percent of cone mass) is practically invariable at each altitude (r.o = -0.11). 

Cone mass and seed quantity achieve their maximum between 300 and 700 m above sea level. Here 

one can observe the highest stability of crops and large numbers of mosaically dispersed patches of 

different seed producing levels. Mean characteristics of Pinus pumila seed production in central and 

eastern Kamtchatka (Table 1, data from 30 sites, confidence level 95 percent, coefficient of variation 

doesn't exceed 28 percent) are as follows: cone length = 42 mm (range: 25 to 62), cone diameter 

= 27 mm (r!Dge: 18 to 37), mean air-dry full cone mass = 7.3 g (range: 4.4 to 10.0), mass of a 

thousand of~--84.4 g (range: 52 to 116), percent of nuclei mass--48 to 54 percent. A typical cone 

includes about 45 seeds, about 39 (range: 26 to 52) seed scales, 11 (5 to 18) of which are undeveloped 

and don't contain seeds. 

Conophagous Insects on Pinus pumila at Kamtchatka 

Pf?lus pumila cones in general, for unknown reasons, are not damaged by a polyphagous cone 

feeders (at least not at Kamtchatka). This may be caused by specific physical and chemical 

characteristics of tree resin which is, in particular, a well-known defense for polyphagous xylobionts. 

Biology of Cecidomyia pumila Mamaev et Efremova sp.n. 

This insect was first recorded on Pinus pumila by LS. Efremova in 1969, but serious difficulties 

in collecting adults and other reasons prevented it from being described as a new species until 1990. 

The description has been made by B.M. Mamaev (in press). The species has never been recorded on 

Table 1. Average properties of Pinus pumila cones at different altitudes in 

the central and eastern Kamtchatka 

Cone Height above sea level- -m 

trait 4 200 400 400 600 650 700 750 900 940 950 1,000 

CM 5.7 5.6 6.7 9.0 9.4 10.0 9.3 9.0 6.6 4.4 5.8 5.7 

SMP 44 45 43 49 45 43 51 55 so 42 46 32 

sss 35 26 42 31 38 43 43 52 42 38 39 40 

sws 12 6 12 5 10 13 18 14 12 10 12 11 

SQT 26 27 40 42 so 46 45 68 54 47 47 so 

SMT 73 100 84 116 94 100 109 78 67 52 75 65 

Note: CM- cone mass, g; SMP- yield (seed mass percent from cone mass), %; 

SSS - seed scale quantity; SWS - quantity of the scales without seeds; 

SQT - seed quantity in a cone; SMT - mass of seed thousand, g; (data are taken 

from various parts of the central and eastern Kamtchatka) 

317 
101 A 681 c 

• • •• • • 

• 

• • • ~ 2. 

- • • • -t• - • 

~ I 2.6 I I I I I • I I I • I I I I I 

a ' 500 iOOO 0 500 1000 

~ 551 )) 68J ]j 

•• • • 

• • ; • • a 

• 

32. 2.6 

0 sao fOOD 0 .500 iQOO 

Figure 1. Seed production dynamics in changing ecotope disposing altitudes (combined data from various 

parts of Kamtchatka Peninsula). Horizontal axis- height above sea level, m. Vertical axis- (A) cone 

mass, g.; (B) seed yield, %; (C) seed quantity in a cone; (D) thousand nuclei mass, g. 
other Kamtchatka conifers. Flying imagos appear in the early July and can be rarely seen in the early 

September even though you can find young and mature larvae in the same cone. Insects feed on the 

first-year cones where adults usually lay about 1 to 5 eggs. In the case of abundant crop, about 

70 percent of cones are occupied by one larva, 20 percent by two, and 10 percent by three larvae. It 

has been noticed that in 50 percent of cases, insects occupy the middle part of the cone, in 30 percent 

of cases--the upper, and in 20 percent--the lowest part. After the hatching a larva bores into the seed 

scale causing the appearance of resin drops on scale surface or between the scales which serve as galls. 

The resin spots are quite visible, and the next year the cone damage is clearly indicated by the surface 

deformation and retarded development of some seed scales. Larvae leave the cones in the middle of 

August and pupate in the soil litter. The insect has a one generation per year. The adult has an 

orange body, with dark thorax and dark, almost black eyes. Male body length is about 2 to 3 mm, 

that of female--3 to 5 mm, the length of wings and legs is about 3 and 5 mm, respectively. Male 

antennae are about half as long as the body. In the laboratory, adults live for about 2 days, both with 

and without food. Insects don't like bright light, they usually die under the lamp heat and prefer 

semi-shadowed sites. Larvae of this genus have cherry-orange or red-orange color, and are 3 to 

4.5 mm long and 1 to 1.5 mm thick. The pupal stage takes about 4 to 5 days in laboratory conditions 

at room temperature. 

Biology of Eupithecia abietaria Goeze. 

This species was first recorded on the Kamtchatka Peninsula by LA Ivliev and D.G. Kononov 

(1962). It has not been recorded on other conifers (Larix kamtchatica, Picea ajanensis). This fact and 

some other reasons cause us to suspect that the Kamtchatka population of Eupithecia is a new species 

because Eupithecia abietaria is well known throughout the palearctic as an oligophagous insect of 

conifers (Stadnitsky et al. 1978). Adults fly from the middle of June, larvae appear in the middle of 

July. Insects feed on the second-year cones. In the year of large crop, a cone is occupied by one 

larva, but in the year of low crop--by two or three larvae. Damaged cones are easily distinguished by 

visible holes and abundant excrements. Larvae feed on seed scales, cone stem, etc., but never on 

mature seeds. They pupate in soil litter in September, and the pupa overwinters. The insect has one 

generation per year. 

Seed Damage by Insects 

Cecidomyia pumila occupies about 70 percent (50 to 100) of Pinus pumila first-year cones in 

various sites and altitudes (Table 2). 

Table 2. Cecidomyia pumila occupation of Pinus pumila cones at central and 

eastern parts of Kamtchatka peninsula 

Height above sea level--m 

Cone trait 10002 Mean 

Percent damaged 60-100 50-70 so 65 100 60 70 

Note: Sites: 1 - sea shore: 2 - subcontinental climatic conditions; 3 - continental climatic conditions (all within the Kamtchatka). 

319 
All estimates are certainly rough because of great variety of habitat conditions, weather, and 

crop yield. Nevertheless, two features were revealed. Firstly, cone damage by Cecodomyia pumila 

varies insignificantly between sites. Second, in the many moderately shaded sites both on the seashore 

and continental climatic conditions, in spite of altitude, the cone damage is substantial in nearly all 

cases. Cecidomyia pumila larvae destroy seed scales thus preventing normal seed development without 

their direct injury to seeds. Defective seed quantity often amounts 20 to 30 percent in a cone. But it 

has been demonstrated that the mean seed quantity in normal and deformed cones appeared to be the 

same. Neither are mean cone diameter and length seriously influenced by the insect injury. Eupithecia 

abietaria, in contrast as has been stressed above, occupies cones during the second summer, in the final 

2 to 3 months of cone development. Very often it chooses cones previously damaged by Cecidomyia 

pumila. The occupation rate is significantly lower than of the previous species and varies from 5 to 10 

percent in the year of large crops to 40 percent in the years of low crop. Eupithecia abietaria prefers 

plains and foothill sites, being rather rare in middle and high mountain sites, i.e. in the main Pinus 

pumila habitats. Its injury does not significantly influence the seed output and cone size. 

CONCLUSION 

Perhaps the main conclusion is that neither insect species damages seeds directly and hence 

cannot seriously influence the seed yields despite their high level of cone occupation. Assuming 

coevolution between producer and consumers, we believe that those cone feeders demonstrate both 

parasitic and commensal relations with the host plant as a whole: parasitic relations prevailing in the 

case of Cecidomyia pumila and commensal one prevailing in the case of Eupithecia abietaria. In 

general, the tree species show sharp antibiosis towards all insects, and only resin-gall species 

Cecidomyia pumila has managed to overcome this threshold very successfully. The main thing is that 

neither this nor the second cone feeding species causes significant injury to the seeds and therefore 

does not influence tree fitness. Taking into account the origin of Pinus pumila in unfavorable and 

even extreme abiotic conditions, it is not surprising to see the host specific gall-forming insect being 

the only one which is apparently fully adapted. Here we see support of the "harsh environment" 

hypothesis (Fernandes and Price 1988), which states that harsh environments favor the evolution of 

gall-forming plant-insect relationships probably due to hydrothermal stresses facing herbivores. The 

"harsh environment" hypothesis seems to favor other kinds of concealed feeders, e.g. xylophages 

Urocerus gigas L. (Hymenoptera, Siricidae) and Pissodes gyllenhali Gyll. (Coleoptera, Curculionidae) 

which feed in dying trunks in the mountain habitats. We admit that Pinus pumila is a young species 

and hence coadaptation with its herbivores and plant neighbors is far from complete. 

LITERATURE CITED 

FERNANDES, G.W. and PRICE, P.W. 1988. Insects galls: adaptations to hygrothermally stressed 

environments? Proc. 18 Inter. Congress of Entomology. Vancouver, 1988. p. 168. 

IVLIEV, L.A and KONONOV, D.G. 1962. About some conifer seed pests at Kamtchatka peninsula. 

Soobschenia DWF SO AN SSSR. Vladivostok. 17: 83-88. (In Russian.) 

STADNITSKY, G.V., JURCHENKO, G.l., SMETANIN, AN., et al. 1978. Insect pests of conifer cones 

and seeds. Vreditely shiskeki semjan khvoinykh porod. Moskwa. 168 p. (In Russian.) 

320 
IPS TYPOGRAPHUS AND OPHIOSTOMA POLONICUM 

VERSUS NORWAY SPRUCE: 

JOINT ATIACK AND HOST DEFENSE 

ERIK CHRISTIANSEN 

Norwegian Forest Research Institute 

N-1432 As-NLH, Norway 

INTRODUCTION 

During the years 1971 to 1982, major epidemics of the spruce bark beetle, Ips typographus L, 

occurred in southeastern Norway and adjoining parts of Sweden. The outbreaks were triggered by 

large-scale wind-fellings and long-lasting drought (Worrell 1983). This "epidemic of the century," 

hitting our important timber tree, Norway spruce, Picea abies (L ), stimulated research in Norway and 

other countries of the region on the relationship between the beetle, its fungal symbionts, and the host 

tree. 

It is assumed that the outcome of a bark beetle attack generally depends on 1) the local density 

of beetles that can respond to aggregation pheromones and 2) the resistance of host trees to attack 

(Berryman 1978, 1982). Field experiments lend support to this hypothesis (Waring and Pitman 1980, 

1983, Raffa and Berryman 1983, Mulock and Christiansen 1986). 

In this paper, I describe the relationship between the spruce bark beetle and its fungal 

symbionts and discuss how the symbiosis enables the beetle to successfully attack living trees. I also 

outline the method by which the trees defend themselves against the joint beetle/fungus attacks and 

discuss the important factors in that defense. 

THE BEETLE-FUNGUS ASSOCIATION 

In the 1970s we discussed with colleagues in the Section of Forest Pathology of the Norwegian 

Forest Research Institute the role that fungi might play in the colonization of trees attacked by 

L typographus. Looking into the literature, we found that there existed a good deal of interesting 

information. 

Discoloration of wood in connection with insect damage had already been noted by Hartig 

(1878), and early in this century bark beetles were directly associated with blue-staining fungi (Munch 

1907, 1908). In 1928 the American forest entomologist F.C. Craighead demonstrated that blue-stain 

fungi play a primary role in the rapid death of pines infested with Dendroctonus beetles. He argued 

that mere girdling by the insects would not kill a tree within a few weeks, since artificially girdled trees 

often live on for months and years. Instead, he suggested, the fungi interrupt the tree's transpiration 

stream, thus causing its desiccation and death. 

BARANCHIKOV, Y.N., MATI'SON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

321 
Following Craighead's suggestion, a number of researchers conducted experiments with American 

pines. Several staining fungi of the family Ophiostomataceae were inoculated into the trees, and in 

some cases caused their wilting and death (Homtvedt et al. 1983). Over the years several 

Ophiostomataceae have been isolated from blue-stained sapwood of Norway spruce (Homtvedt et al. 

1983, Solheim 1986). An early attempt to establish some of these fungi in spruce trees through 

artificial inoculation proved futile (Munch 1907, 1908). 

In 1980 our pathologist, Richard Homtvedt, decided to try an inoculation experiment using two 

Ophiostoma ( = Ceratocystis) species that had frequently been mentioned as associates of the spruce 

bark beetle, Ophiostoma piceae H. and P. Syd. and 0. penicillatum Siem. Three cambium-deep girdles 

were cut around the stem of each tree. Cotton ropes soaked in agar and thoroughly infected with the 

fungi were placed in the girdle and covered by tape. The experiment failed as Munch's had done; no 

fungal infection of the xylem could be observed. 

At this time a mycologist, Halvor Solheim, had just joined our group to study the succession of 

microorganisms in beetle-killed spruce trees. He soon made a very significant discovery: the species 

Ophiostoma polonicum Siem., to which no one had hitherto paid much attention, was always found at 

the advancing front of blue stain in the sapwood of beetle-attacked trees. In 1981 we inoculated both 

0. polonicum and 0. penicillatum under the bark of young and old spruce trees, using the cork-borer 

technique (Wright 1935) and infected wood-chips inserted under the bark (Reid et al. 1967). The 

inocula were placed 2 em apart along rings encircling the stem. We discovered that 0. polonicum, but 

not 0. penicillatum, was able to kill trees of normal health. It penetrated sapwood of normal water 

contents, and in doing so caused a blockage of the transpiration stream through the stem (Homtvedt 

et al. 1983). 

Repeated experiments have verified that 0. polonicum will kill healthy spruce trees provided an 

adequate load of inoculum is given (Christiansen and Homtvedt 1983, Christiansen 1985a, 1985b, 

Christiansen and Ericsson 1986, Homtvedt 1988, Solheim 1988). On the other hand, further studies 

confirmed that our isolates of 0. penicillatum and 0. bicolor are unable to kill trees of normal health 

(Solheim 1988). The differences in pathogenicity between the fungal species can probably be explained 

by their differential abilities to colonize wet sapwood. 0. polonicum seems to tolerate low oxygen 

conditions better than the other species mentioned here and consequently also tolerates a wetter 

growth substrate (H. Solheim, pers. comm. ). 

The relationship between 1 typographus and its fungal symbiont is an example of true mutualism, 

since both parts benefit from it. The pathogenic fungus helps the beetles kill trees, thus making them 

available for beetle reproduction. The benefit for the fungus is transportation to new hosts and 

effective inoculation under the bark. Since the mutualists have joined forces in such a deadly way, 

there must be a means by which the trees defend themselves against attack, thereby securing their own 

future existence as well as that of the parasites. 

DEFENSE MECHANISMS OF THE TREES 

Coniferous trees have coevolved with insects and parasitic microorganisms, including fungi, for 

over 200 million years. To survive they have developed effective systems of defense. Whereas a tree 

can lose large parts of its crown and root biomass and still survive, loss of the cambium around the 

stem constitutes a mortal threat. In several important conifers, the defense of stem tissues is based 

upon secretion of resinous materials. 

"Resin" in its broadest sense has long been regarded as important for the defense against bark 

beetles in Norway spruce (Gmelin 1787) and other conifers. The pioneering work of Reid et al. 

(1967) on lodgepole pine, Pinus contorta, in Canada added a new dimension to the concept. It became 

clear that the resin observed in the case of beetle/fungus attack has two different origins: on the one 

322 
hand, there is the preformed (or "constitutive") resin in ducts in the bark and sapwood, and on the 

other hand, there is the resin produced by an induced reaction to wounding and infection. The two 

types of resin are termed "primary" and "secondary," referring to the order of their appearance in the 

tree. 

Preformed Resin: The "Standing Forces" 

Preformed resin originates from an interconnected system of ducts in the phloem and xylem. 

This system comprises the "standing forces" of the tree, which become operative once a resin duct is 

severed, e.g. by a mining beetle. After the resin has been flowing for a short period of time, its 

surface will crystallize to form a hard, protective surface over the wound. A system of resin ducts 

exists in some coniferous genera (e.g. Larix, Picea, Pinus, and Pseudotsuga), but is absent in others 

(e.g. Cedrus, Sequoia, and Thuja). Abies species have resin blisters in the bark, but these can in some 

cases be avoided by bark beetles (Ferrell 1983). 

The preformed resin has been subjected to extensive studies in pines, partly in connection with 

its commercial use. Investigations related to bark beetle attack on ponderosa pine have emphasized 

the importance of oleoresin exudation pressure (OEP) because OEP would influence the quantity of 

resin that an attacking beetle would have to cope with (Vite 1961, Vite and Wood 1961). Because 

OEP is often correlated with the turgor pressure of the epithelial cells surrounding the resin ducts, 

droughty conditions could lower OEP and possibly facilitate beetle attack. 

Studies of pines in the southern U.S.A have, however, indicated that the exudation flow (OEF) 

largely depends on the storage capacity of the resin duct system and the viscosity of the resin, whereas 

OEP seems to be less important (Hodges and Lorio 1971). It seems logical to assume that OEF and 

total quantity exuded are the critical factors for an attacking beetle. The formation of resin ducts 

seems likely to be influenced by the growth-differentiation balance of the tree (Lorio 1986). 

Induced Resinosis: The "Mobilization Defense" 

Preformed resin may repel, flush out, and even drown attacking beetles. If these "standing 

forces" of the tree are inadequate for arresting the beetles, however, the phloem, cambium, and outer 

sapwood become infected with propagules of microorganisms. Most important of these are the spores 

of blue-stain fungi, which are specially adapted for transportation by insects by being covered with an 

adhesive, mucilaginous sheath. After these spores germinate, the fungus may soon spread into the 

surrounding tissues. It has been pointed out that since the preformed resin does not permeate the 

host tissues in advance of fungal growth, it is unlikely that it can prevent the spread (Berryman 1972). 

When infected by microorganisms, whether fungi, bacteria, or vira, most plants have a 

hypersensitive reaction (Klement and Goodman 1967). A necrotic area forms around the point of 

infection so that the invading organism is deprived of food. Such necrotic reaction zones forming in 

the cambial region of conifers may also become impregnated with resinous and phenolic compounds, 

which creates an environment very unfavorable to beetles and fungi (Reid et al. 1967, Berryman 1969, 

Shrimpton 1973, Wong and Berryman 1977). The wound resin is produced by living parenchyma cells 

of the phloem and sapwood, including new-formed callus parenchyma. It is synthesized from 

carbohydrates stored in parenchyma cells of the phloem and xylem (Reid et al. 1967, Shrimpton 1978, 

Cheniclet et al. 1988, Lieutier and Berryman 1988), the reaction being elicited by substances produced 

by the fungus (Lieutier and Berryman 1988). 

The induced response constitutes the "mobilization forces" of the defense, which come into 

action more slowly, but can stay active for an extended period of time. In lodgepole pine, where this 

reaction has been studied most intensively, it is considered the main defense against bark beetle attack, 

323 
the preformed resin merely delaying the beetles and allowing more time for the secondary response 

(Raffa and Berryman 1982). The induced response is concentrated in a small area surrounding the 

infection, thereby keeping the loss of cambium to a minimum (Raffa and Berryman 1982). The 

process is highly energy-demanding (Wright et al. 1979) and probably related to the overall vigor of the 

host tree (Raffa and Berryman 1982). 

STUDIES OF THE DEFENSE IN NORWAY SPRUCE 

In 1983 we carried out a field experiment to establish the number of L typographus attacks 

necessary to kill a Norway spruce tree (Christiansen 1985b). Pheromone dispensers were attached to a 

number of trees, and shortly after the main flight of the beetles, the number of attacks was recorded. 

In several trees, the attack appeared to be successful, only dry frass being expelled from the 

entrance holes. However, about 1 month after attack, we observed that liquid resin was now seeping 

from formerly dry holes. Removing the outer cork bark, we found resin-impregnated reaction zones 

surrounding egg galleries of different lengths (Fig. 1). Obviously, the preformed resin had been 

inadequate to prevent the beetles from excavating their nuptial chambers and initial egg galleries. 

Later, however, secondary resinosis had put an end to the breeding. This was one of the reasons why 

we wanted to take a closer look at the relative importance of the two defense systems in Norway 

spruce. 

The Preformed Defense 

Schwerdtfeger (1955) studied the efficiency of the resin duct system under different conditions by 

making cambium-deep cuts of a standard size in the bark and measuring resin exudation within a 

maximal period of 3 days. One of his conclusions was that the quantity of resin exuded by a standard 

wound in the phloem-cambium region will rapidly taper off when the number of wounds increases. He 

also established a clear seasonality in resinosis, the quantity of exudate showing a strong positive 

correlation to ambient temperature. The amount of preformed resin exuding from a mechanical wound 

varies greatly from tree to tree, and even between places on a given tree (Christiansen and Homtvedt 

1983). Within a stand, there is a trend toward a higher yield of duct resin per wound among the 

larger trees (Fig. 2), also suggested by Schwerdtfeger (1955). Likewise, older trees seem to exude at 

least as much resin as younger (Schwerdtfeger 1955, Christiansen and Homtvedt 1983). 

There are several sources of seasonal and annual variation in amounts of duct resin. Newly 

formed resin ducts of the sapwood may not become connected with phloem ducts until most of the 

year-ring has been laid down, as observed in pines (P.L Lorio, Jr., pers. comm. 1986). Also, different 

year-rings of Norway spruce may hold highly variable numbers of resin ducts, which can be formed in 

response to external stresses, i.e. frost, drought, or attack by insects and fungi. During extremely dry 

years of the mid-1970s, unusually high numbers of ducts were formed in connection with drought rings 

in the spruce trees we examined. Due to this variability, pioneer beetles may encounter "standing 

forces" of variable strength depending on where and when they attack. 

An experiment we conducted in Norway in 1985 sheds some light on the relative importance of 

the two defense systems. It was just after the recent large epidemic and very few trees were 

spontaneously killed by L typographus that year. In the experiment, pheromone dispensers were 

attached to 77 spruce trees of variable vigor. All 77 came under attack, but only 20 of them died. 

Shortly after the main flight of the spruce bark beetle, we counted the number of attacks on each tree. 

In doing so, we distinguished between entrance holes where liquid resin or moist frass occurred and 

holes where only dry frass was expelled. Very few attacks occurred after this major inspection. 

324 
Figure 1. The spruce bark beetle has been able to enter the phloem and 

initiate its galleries without being stopped by the preformed resin of the 

tree. Later, however, the induced defense has produced abundant resin that 

permeates the phloem locally around the galleries. The eggs have been killed, 

and the fungus is contained inside the resin-soaked areas. 
mm 

25 • 

Wood Ill/Ill~ • 20 Ill flll I 

Bark 

• • 

15 • • • • 

• 

• • • I • 10 •• • 

• • • • •• • • • • • • • • I . : • 

••• • 

5 • • • .. • • 

I • • • • • :. .. 

.. .. •'. I I • I • I • ..l- I -:. • •• • .. .. • 0 -· ...... -·. • 

lO 20 30 em DBH 

Figure 2. The inserted drawing shows measurement of the yield of constitutive 

resin: plastic tubes are cut at an angle and fitted into holes cut to the 

cambium with a cork borer. After 24 hr the length of the resin column is 

measured. The main figure gives mean values of 10 measurements per tree for 

128 spruce trees growing in a small stand. 

There was great variation in total number of attacks per tree (Fig. 3). Surviving trees showed a 

maximum of about 500 entrance holes, whereas killed trees had no less than 200 to nearly 1,200. In 

the killed trees only a small percentage of the boring holes had resin exudation; the proportion was 

almost zero in some trees. Surviving trees had fewer attacks in general and a higher, but extremely 

variable proportion of holes with primary resin. On one of these trees, over 300 boring holes were 

recorded, all of which were oozing resin, whereas in others only a small share of the entrance holes 

exuded resin. 

Although the results mentioned here are only fragmentary, I think it is safe to conclude that the 

"standing forces" of the resin duct system are inadequate as a sole defense against a mass attack of 

L typographus. It should be pointed out that in other trees, such as certain pines, this first line of 

defense may be much more important (Christiansen et al. 1987). 

326 
100 

% CDOQ)CID 

C!ID 

80 crooo 

0 0 0 

C!D 

60 OCD 

00 

0 

0 

40 0 0 

co 0 

0 •• 0 

20 croo 

0 (X) .. • • oe:JD • • 0 ••• •• • 

0 250 500 750 1000 1250 

Total number of attacks X 20/DBH 

Figure 3. Performance of the constitutive defense in Norway spruce: percent 

of beetle entrance holes with liquid resin or resinous frass in relation to 

total number of attacks per tree. Black circles - trees killed by the attack; 

white circles - trees surviving. 

The Induced Defense 

The induced defense reaction in Norway spruce has been studied using artificial inoculations 

with 0. polonicum. It turns out that other Ophiostoma species will produce reactions of a similar type 

(Horntvedt et al. 1983, Solheim 1988), but we have concentrated on 0. polonicum, which is able to 

penetrate the sapwood and kill experimental trees. 

Artificial inoculation offers an interesting opportunity for experimental study of the relative 

resistance of individual trees. By using this technique, we can administer exact numbers of infections 

to a given tree. Theoretically, this can also be achieved by subjecting the tree to a controlled number 

of beetle attacks. In practice, however, it is very difficult and laborious because the experimental 

beetles inevitably attract "wild" conspecifics to the tree. Thus the part of the bole which is suitable for 

L typographus would have to be screened in order to prevent unwanted attacks. 

It is possible that the reaction of a tree to one single inoculation could be used as a predictor 

of its resistance to mass inoculation, as demonstrated for lodgepole pine (Raffa and Berryman 1983). 

This might possibly be used to assess resistance to beetle attack as well. In our experiments, however, 

we have studied only the tree's reaction to mass inoculation. Our technique has been to mark out a 

belt on the stem, 60 or 80 em high, around breast height. Within this belt, the trees are inoculated at 

327 
different densities, ranging from one to eight inoculations per square decimeter. A template is used to 

ensure even spacing of the points of inoculation. Alternatively, the inocula are placed along rings 

encircling the stem, virtually covering the same area as the inoculation belts. The cork borer technique 

has been used as a standard. Placing the inoculations so densely within a limited area, instead of 

spreading them out over a larger section of the bole, is considered a "worst case" for the defense. 

However, a pilot study in which an equal number of inoculations was given over 60, 120, or 240 em of 

the stem did not reveal any dramatic differences in fungal success (unpubl. data). 

The experiments have demonstrated a clear threshold of successful infection (Christiansen 1985a, 

1985b ). When the number of infections in a tree increases, there is a point where the resin 

concentration of the phloem reaction zone drops (Fig. 4). At this critical point, the fungus is able to 

break out of the enclosure and spread out into the phloem. This is parallelled by increasing success of 

the fungus in penetrating the sapwood. 

There also appears to be a difference in defensive capacity between spruces of different vigor. 

Suppressed, slow-growing trees appear to tolerate fewer infections than dominant and vital ones 

(Christiansen 1985a). This accords with a study of host resistance to L typographus attacks by Mulock 

and Christiansen (1986). 

Role of Carbohydrates in the Induced Defense 

From the threshold response described above, it may be inferred that defensive capability is 

influenced by the availability of some limited resource. Since it is known that carbohydrates (C) are 

both raw material and energy source for the wound response, availability of C in the infected area 

would seem one likely candidate for a critical factor. I have tested this assumption experimentally 

(Christiansen and Ericsson 1986). Our first hypothesis was that if substantial amounts of sugar are 

mobilized for the induced defense, then C (starch) reserves of the surroundings should be depleted. 

Second, we assumed that trees with low reserves should be more vulnerable to fungal attack than trees 

with high starch concentrations. 

We inoculated spruce trees in belts as described above, and measured the starch concentrations 

at different distances above the belt. Our first hypothesis was supported in that starch concentrations 

were significantly reduced as far as 1.5 m above the inoculated belt. But the experiment failed to 

support our second hypothesis. Trees ranging from 12 to 20.7 percent in starch concentration showed 

no differences in defensive capacity. Similar results were found in a later investigation (Homtvedt 

1988). 

In a second experiment (Christiansen and Ericsson 1986), we girdled some of the trees above 

the inoculation belt to manipulate their starch reserves. A cambium-deep girdle at 2 m above ground 

shut off the assimilate flux from the crown. One group of trees was girdled in April, before the spring 

build-up of C reserves. In these trees the starch concentration reached only half the normal (Fig. 5). 

Another group was girdled at the time of inoculation (i.e. mid-May) and consequently had normal 

starch reserves. In this experiment we had carefully chosen our inoculation dose so that inoculated, 

ungirdled trees withstood the infection quite well; only a small fraction of their sapwood became blue 

stained (Fig. 5). Low-starch (i.e. early-girdled) trees were much more stained, but so were trees girdled 

at the time of inoculation. We therefore concluded that it may not be the size of the C reserves 

(starch) per se, but rather the efficacy of C (sugar) translocation that is critical for the mobilization 

defense. Our conclusions are corroborated by a study of lodgepole pine in the U.S.A (Miller and 

Berryman 1986) performed simultaneously, but independently. 

328 
30 

20 

0 

RESIN 

CONCENTRATION 

1 2 

I 

8 

100~~--------~----------~--------~~ 

50 

BLUE-STAINING 

OF SAPWOOD 

o~~------------------------~----------~~~ 

1 2 4 8 

Inoculation density 

Figure 4. Performance of the induced defense in Norway spruce: resin 

concentration in phloem reaction zones and fungal success in relation to 

inoculation density. Data from Christiansen 1985a. 

329 
20 

% 

15 

10 

• D 

0 

• 

5 

10 

PHLOEM 

STARCH 

CONCENTRATION 

April May June 

SAPWOOD 

BLUESTAINING 

Figure 5. Starch dynamics of Norway spruce in relation to fungal inoculation 

and girdling of the stem and fungal success in invading the sapwood. Data 

from Christiansen and Ericsson 1986. See text for further explanations. 

During the growth season, many sinks compete for the available C in a tree. Priorities for 

C allocation seem to exist. In a defoliation experiment with Scots pine, Eriason et al. (1980) found 

the following order of allocation (moving from high to low priority): 1) bud formation, 2) needle 

biomass, 3) shoot length, and 4) year-ring width. Allocation for defense may not be the highest 

priority (Waring and Pitman 1985), but a high drain on C by numerous induced defense reactions 

considerably affects year-ring growth in Norway spruce (Christiansen 1985a). 

Since carbohydrate availability varies during the growing season (e.g. Eriason et · al. 1980), this is 

likely to affect the defensive capacity of the trees. An experiment with monthly inoculations of Norway 

spruce showed considerable variation in defensive efficacy over the season (Homtvedt 1988). The 

success of 0. polonicum in infecting the sapwood was very low in May, moderate in June, and high in 

July, then declined through August and September. The lack of fungal success in spring could not be 

explained by lower temperatures only; the trees were evidently more resistant in the early season. 

Because L typographus has its main flight in spring (mid-May in South Norway), the beetles 

appear to encounter host trees in a highly resistant state. Nevertheless, they are able to overcome the 

resistance of the host given an adequate number of attackers. On the other hand, during an epidemic, 

when the parent beetles produce one or more sister broods, increasing susceptibility late in the season 

may reduce the number of beetles necessary to kill a tree. This may have a bearing on population 

dynamics, as pointed out by Homtvedt (1988). 

It has been suggested that tree resistance in general may be closely related to the amount of 

photosynthate that is immediately available for defense (Christiansen et al. 1987). A wide variety of 

330 
factors is known to predispose trees to bark beetle attack, among them drought, flooding, wind-swaying, 

defoliation, lightning strike, fire, rot fungi, competition, and old age. These seemingly unrelated factors 

may have a common denominator: they all reduce the C availability. It would thus be interesting to 

test the relationship between limitations on the transfer of C to the sites of attack and host tree 

resistance. 

At present, we are testing this hypothesis in experiments with Norway spruce. We are trying to 

reduce C stores--and hence, presumably, availability--by two techniques: 1) by exposing the trees to 

prolonged drought and 2) by reducing the crown biomass considerably through branch pruning. Later 

the trees will be inoculated with 0. polonicum to test their resistance. 

EPILOGUE 

Together, the two defense systems will define the "threshold of successful attack" for a given 

tree. Both defenses become exhausted when the number of attacks reaches the critical level. Given 

the high population densities of an epidemic, any tree can be killed in a mass attack. When the trees 

are rapidly overwhelmed by a large number of beetles, no constitutive defense will suffice and no 

evidence of the induced defense can be observed, as there is no time for the reaction to take place. 

Even though the described defense mechanisms are no safeguard during an epidemic, they do 

protect the spruce trees in a normal situation. They prevent the tree from being conquered by a 

handful of attackers, and they contribute to reduction of the beetle population. Since at least the 

induced defense reaction seems related to the vigor of the host tree, the forest manager can probably 

reduce the possibility of beetle outbreaks by maintaining a vigorous forest. 

SUMMARY 

This paper describes the relationship between the bark beetle Ips typographus and its fungal 

symbionts, in particular Ophiostoma polonicum, attacking Norway spruce, Picea abies. Against a joint 

beetle-fungus attack, coniferous trees defend themselves by means of 1) their preformed (constitutive) 

duct resin and 2) an induced reaction producing highly resinous zones around the points of infection in 

bark and outer sapwood. The performance of the two defense systems is discussed, with particular 

reference to Norway spruce. The importance of carbohydrate availability for the induced defense 

reaction is discussed. 

LITERATURE CITED 

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GMELIN, J.F. 1787. Abh. Wurmtroknis. Crusius'sche Buchhandlung, Leipzig. 

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HORNTVEDT, R., CHRISTIANSEN, E., SOLHEIM, H., and WANG, S. 1983. Artificial inoculation 

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332 
LORIO, P.L, Jr. 1986. Growth-differentiation balance: a basis for understanding southern pine beetle 

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297-323. 

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334 
RELATIONS BETWEEN WOOD-INHABITING 

INSECfS AND FUNGI 

NINA P. KRNOSHEINA 

AN. Severtzov Institute of Evolutionary Animal Morphology and Ecology 

U.S.S.R. Academy of Sciences 

Moscow 117071 U.S.S.R. 

INTRODUCTION 

It is widely known that xylophagous insects do not usually attack healthy, resistant trees. In 

order to overcome these defenses, inner-bark feeding insects have developed symbiotic interrelationships 

with various organisms, fungi in particular. In this paper, using our own data together with that 

available in the literature, we analyze the forms of relationships between insects and fungi and the role 

of these interactions at various stages of wood decomposition. In doing so, we distinguish between the 

following fungal-insect relationships: 

1) ambrosia mycetophagous insects, symbiotically associated with primary ambrosia fungi 

2) ambrosia xylomycetophagous (phloeomycetophagous) insects, symbiotically associated with 

wood-coloring fungi (auxiliary ambrosia fungi according to Batra 1985) 

3) xylophagous insects, symbiotically associated with fungi causing vascular mycoses 

4) destructive xylo-, mycetophagous insects, associated with wood-destroying fungi. 

The representatives of the first three groups develop in living wood or fresh timber. Representatives 

of the last group develop in dead wood, though in the earliest stages they can colonize living, but 

irreversibly weakened wood. 

REVIEW 

Ambrosia Mycetophagous Insects 

This group includes insects which have necessary ectosymbiotic connections with a specific group 

of fungi imperfecti, the ambrosia fungi, and several characteristic features. The ambrosia fungi are 

highly sensitive to drought and develop only in moist wood. They are host specific, associated with 

certain species of insects, and are located only in colonized galleries or on the body of xylobionts. The 

fungi form the pellicle on the gallery walls--ambrosia--consisting of separate cells and fragments of 

filaments (Batra 1985 and others). Ambrosial cells can form vegetative mycelium under certain 

conditions. 

Typical representatives of the ambrosia fungi are Ascoidea, Ambrosiella, Rajfaelea, and 

Phialophoropsis (Batra 1967, 1985). The taxonomy of this group of fungi is poorly studied, 

representatives of other ecological groups, considered by us below, often being confused with them. 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

335 
Typical representatives of the ambrosia insects group are Platypodidae, Lymexylonidae, and some 

Scolytidae--XyleboiUS Eichh., Trypodendron Steph., and Anisandrus Ferr. (Francke-Grosmann 1967, 

Nakashima 1971, 1972, 1975, Mamaev 1977, Batra 1985, Nakashima et al. 1988). Some peculiar beetle 

representatives, Curculionidae and flies--Axymyiidae and Syrphidae--should also be classed among this 

group. The complex of ambrosia mycetophages is formed on both living wood and fresh timber. It 

has been said of the pin hole borer, Austroplatypus incompertus (Schedl.), that one and the same system 

of galleries can be used over 36 years (Harris et al. 1976). Ambrosia fungi have been obtained from 

the galleries of borers, pin hole borers, and bark beetles (Lyme:xylonidae, Platypodidae, Scolytidae) 

(Francke-Grosmann 1967, Baker and Norris 1968, and Nakashima 1971). 

It has been ascertained that ambrosia fungi constitute the main food source for ambrosia insects 

(Kaneko and Takagi 1966, Norris and Baker 1967), and this determines insect behavior. The bark 

beetle Xylosandrus compactus Eichh. (Scolytidae) lays eggs only during the four to 14 days after 

colonization of the trunks of the coffee tree, i.e. after spreading of the ambrosia fungus mycelium 

throughout the surface of the gallery (Hara and Beardsley 1979). Successful larval development and 

imago reproduction are determined mainly by insect feeding on the ambrosia fungi (French and Roeper 

1972, 1975, Barras 1973). Mamaev (1966) considered ambrosia insects xylomycetophagous. However, 

recent data show convincingly that they should be considered ambrosia mycetophages. This 

identification is indirectly confirmed by the peculiar intestinal structure of Axymyiidae larvae, without 

additional chambers or folds, which is pronounced in xylophages (Mamaev and Krivosheina 1966). 

Apparently ambrosia insects are associated with fungi on a large number (up to 150 species) of 

host trees (Francke-Grosmann 1967). Colonization of new tree species occurs fairly quickly. For 

example, the ambrosia beetle, Xylosandrus compactus Eichh., was at first primarily on coffee trees on 

the Hawaiian Islands, but then spread throughout more than 100 tree species there (Hara and 

Beardsley 1979). 

Symbiotic connections with fungi lead to the formation in ambrosia insects of various structures 

for the transfer of fungi. These structures are known as mycangia or mycetangia and are situated on 

the body and in the internal organs. The organs have been studied well enough in bark beetle pinhole 

borers and have also been found in the attelabid beetles (Schneider 1976, Nakashima 1975, Sawada and 

Morimoto 1986). The synchronization of insect and fungi development is also of interest. It was 

discovered in Corthylus punctatissimus Zimm. (Scolytidae) that ambrosia fungus, Amabrosiella xylebori, 

reproduces intensively by gemmation in mycangia only prior to wood colonization by beetles (Roeper 

1988). 

In the European part of the U.S.S.R., the complex of ambrosia insects is represented by the 

borers Elateroides dermestoides L. on deciduous trees and E. flabellicomis Sch. (Lymexylonidae) on 

conifers. Usually they are accompanied by the larvae of Libnotes Westw. (Limoniidae). The bark 

beetles XyleboiUS Eichh., Trypodendron Steph., and Anisandrus Ferr. are often found together with the 

borers (Mamaev 1974b, 1977). Platypus cylindriformis Rtt., which is close to the more widely 

distributed P. cylindrus Hbst. (Platypodidae), develops in oak stumps in the Transcaucasus region. The 

ambrosia insect complex in the forests of the Far East (U.S.S.R.) is the most diverse, however. The 

most common ambrosia insects are Platypus severini Bl. (Platypodidae) and Sipalinus gigas Fabr. 

(Curculionidae), which occupy various tree species: cedar, fir, elm, and lime (Mamaev 1974a). 

The ambrosia dipterans complex forms in moist dying or dead wood. It is represented by 

species of Axymyiidae, Syrphidae (Temnostoma St. Farg et Serv.) (Fig. 1a ), Stratiomyidae 

(Xylopachygaster Kriv. ), and Limoniidae (Libnotes Westw. ). 

Axymyiidae larvae colonize newly felled trunks, where they may exist for several years in the 

moist conditions. The larvae construct galleries, constantly removing boring dust and fungi. Both 

larvae and pupae are mobile, the latter having a sclerotized flat cover on the head for clearing galleries 

(Fig. 1). 

336 
A similar life pattern is typical to the species of the genus Temnostoma St. Farg. et Serv. 

(Syrphidae), which occupy the fresh wood of fallen trees. The peculiar keg-like shape of their larvae's 

bodies helps them to clear galleries (Fig. 1c). 

Unfortunately, the composition of the fungi communities in the galleries of Ambrosia dipterans 

and the mechanism of their transfer have not yet been studied. It is very likely that, in addition to 

ambrosia fungi, yeast is of great importance there. The species of the genera Libnotes Westw. 

(Limoniidae) and Xylopachygaster Kriv. (Stratiomyidae) associate only with ambrosia insects and do not 

take part in fungi transport. 

Ambrosia Xylomycetophagous (Phloeomycetophagous) Insects 

The ambrosia xylomycetophagous insects are consistently associated with the cup and imperfecti 

fungi (micromycetes). The latter consume chiefly the contents of the cells and do not destroy cellular 

walls, though these traits do not strictly define them (Gorshin and Krapivina 1969). 

Unlike the ambrosia fungi, the wood-coloring fungi are not closely associated with insects, 

appearing in the galleries after completion of insect development. Easily cultivated, they can be 

mistaken for ambrosia fungi because they are often associated with them. 

The most typical representatives of this group are the Ceratocystis, causing the blue-stain disease 

of the wood. The spores of the blue-stain fungi are spread by the air flow and by xylobiont insects, 

particularly when insects transfer sticky secondary spores of the cup fungi (Beliakova 1954, Batra 1985). 

Wood-coloring fungi infest weakened, drying, and newly felled trees, which are characterized by the 

high humidity of wood and large amounts of easily assimilated substances. 

Close connections between wood-coloring fungi and bark beetles of the genera Dendroctonus Er, 

Ips Deg., Pityogenes Bed., Hylastes Er., and Hylurgops Lee. have been established (Mathre 1964, 

Francke-Grosmann 1967, Barras and Perry 1971, Raffa and Smalley 1988, Furniss et al. 1988, and 

Bennet and Tattar 1988). 

It is possible to observe mutualistic interactions between wood-coloring fungi and bark beetles. 

The wood infested by blue-stain fungi is the most attractive and accessible to the bark beetles (Goheen 

et. al. 1985). This can be explained by several facts. The fungi facilitate wood assimilation by the 

insects and promote xylophage aggressiveness, and fungi activity is known to increase the protein 

content of the wood (Hodges et al. 1968) and to decrease the water supply (Horntvedt at al. 1983). 

Together this results in the most favorable conditions for bark beetle development. On the other 

hand, mutualistic interactions promote special adaptations for fungi transmitting (Barras and Perry 

1972, Furniss et al. 1988). The mechanism of fungi transfer is not simple. Secondary spores are fixed 

not only in mycangia, but directly on the body surface as well (Barras and Perry 1972, Livingston et al. 

1983, Paine and Birch 1983). 

Some data testify to the complex interactions between the ambrosia fungi and the ambrosia 

xylomycetophagous insects. The connection between tree colonization by bark beetles and intensive 

mycelium growth in mycangia was noted by Paine and Birch (1983). The bark beetles inoculate the 

wood with several Ceratocystis species. At the same time, however, the species preventing intensive 

blue-stain fungi development and favoring beetle breeding are also transferred in mycangia (Bridge and 

Perry 1985, Wood et al. 1988). 

The interactions between bark beetles and wood-coloring fungi are considered by some authors 

to be facultative (Mamaev 1977, Batra et al. 1985). That supposition is partially confirmed by the 

peculiarities of the ecology of the fungi--they can develop without interactions with insects--and by 

337 
Figure 1. Preimaginal stages of xylobiont dipterans. A - the larvae of 

Mesaxymyia kerteszi Duda (Axymyiidae), B- the fore end of the head of pupa 

Mesaxymyia kerteszi Duda (Axymyiidae), and C- the larvae of Temnostoma 

vespiforme L. (Syrphidae). 

features of the ecology of the insects--their capacity for development without symbiotic fungi has been 

documented (Grosmann 1931, Holst 1937). At the same time, more recent data do not resolve this 

question definitively. The bark beetles of this community feed on wood infested by fungi. We classify 

these beetles as xylo- or phloeomycetophages. 

Xylophagous Insects Associated with Vascular Mycoses 

Vascular mycoses are common among elms (Ulmaceae) and beeches (Fagaceae) and are caused 

by Ceratocystis fungi. The most familiar is Dutch elm disease, caused by the fungus C. ulmi. Among 

its vectors are now considered all the species of Scolytus Geoffr., the species of Pteleobius Bed., 

Hylurgopinus rujipes Biehn., the weevil Magdalis armigera Geoffr. (Curculionidae), and the capricon 

beetle Saperda punctata L (Cerambycidae) (Pfeffer 1979, Bejer 1979, Covassi 1980, Sengonca and 

Leisse 1984). The insects infect living trees during their feeding in the crown. Dying of the branches 

and tree weakening create favorable conditions for occupation of the stems by the insects. A similar 

disease causing oak mortality is widely distributed throughout Europe and North America. The 

pathogen of oak mycosis in the U.S.A is Ceratocystis fagacearum (Rexrode and Jones 1970, 1971); in 

Europe it is the species of Ceratocystis, Diaporte, and Fusarium (Kriukova and Plotnikova 1979, 

Kuzmichev 1982). The bark beetles Pseudopityophthorus minutissimus Zimm., P. pruinosus Eichh., and 

Scolytus intricatus Ratz. are considered vectors. In recent years, the role of sap beetles (Nitidulidae) in 

fungi transmitting has been discussed (Appel et al. 1986). These diseases caused by insect vectors are 

338 
likely to be distributed widely. Accordingly, the role of Platypus subgranosus Schedl. as a Chalara 

australis vector causing the drying wilt of beech myrtle (Fagaceae) has recently been identified (Elliott 

et al. 1988). Similar interactions have been observed between the sawyer beetle, Monochamus urussovi 

Fisch., and the fungi, Ceratocystis spp. (lsaev et al. 1988). Isaev et al. (1988) attach no less importance 

to these fungi than to the well-known pathogen of Dutch elm disease. 

Infection of the beetle by the secondary spores takes place in the pupal chamber, on the walls 

of which the perithecium develops. Coincidence of the development cycles of both fungus and insect 

points to the historical connections between these species. Thus Vasechko (1981) and Lindeman 

(1986) thought this fungi to be an adventive species, against which the trees have not yet developed a 

pronounced resistance. It is possible, however, that the cause of such wide disease distribution is 

sufficient pathogen variability; if anything, it is represented now by several strains (Bazzigher 1981 ). 

There are essential differences in the interactions between the fungi and the ambrosia 

xylomycetophages communities associated with wood-coloring fungi and those of the xylophages 

associated with vascular mycosis pathogens. In the first case, the bark beetle galleries occur on the 

trunk sections infected by the blue-stain fungi or in the parts nearby. In the case of vascular mycosis, 

there is asynchrony of trunk colonization by fungus and insects. With respect to insects, the fungi are 

a factor of tree weakening. As a result, insect species of this community have neither trophic nor 

biotopic connections with fungi and are typical phloeoxylophages. 

It is important to remember that two ecologically distinct groups of fungi, having qualitatively 

different connections with insects, exist within the genus Ceratocystis. 

Destructive Xylomycetophages Occupying Mainly Dead Wood 

Wood-destroying fungi affect cellulose and lignin--the main components of the ceU walls--

causing wood rotting. Various species of fungi are characterized by different selectivity, causing rots 

distinct in color and structure: corrosive or destructive, brown or light. In the final stages of a tree's 

decay, the xylophagous insects prefer destructive light and brown rots. The greatest numbers of 

wood-destroying fungi are among the basidium fungi, but trunk rot is caused by cup and imperfecti 

fungi as well. 

Insects associated with wood-destroying fungi can be placed in three large· groups: speciesvectors of fungi, which are not trophically related to infected wood; species transferring the fungi 

spores and preparing the substrate for their brood; species trophicaUy related to fungus infecting the 

wood, but lacking special structures for fungi transfer. Representatives of the first group, while 

promoting wood-destroying fungi development, weaken trees and create conditions favorable to 

xylophage breeding. 

Up until now, not enough attention has been paid to the role of insects in the transferring of 

wood-destroying fungi. The assumption has often been made that the role of the bark beetles is 

secondary, only associated with wood-destroying fungi (Beaver 1976). In fact, however, much data 

document bark beetles--Dendroctonus Er., Hylurgops Lee., Ips Deg., Scolytus ratzeburgi Jans.--occupying 

trees infected by tinder or gill fungi (Livingston et at. 1984). At the same time the role of 

Dendroctonus in transferring spores of Fomitopsis pinicola has been demonstrated by Harrington et at. 

(1981). The connection between the bark beetles D. ponderosae Hopk. and Pityogenes fossifrons Lee. 

and tree infection by the honey-fungus Armellaria me/lea was discovered by Kulhavy et al. (1984). Bark 

beetles and weevils, particularly Hylobius abietis L., are thought to be vectors of the pine-fungus 

Fomitopsis annoosa (Nuorteva and Laine 1968). The role of the representatives of the above 

mentioned group in the tree-fungus-insects system is not simple; they are likely to be both fungi 

associates and their vectors. 

339 
Typical representatives of the second species group, transmitting fungus infection and preparing 

the substrate for brood development, are the horntails. A connection has been found between 

horntails and the fungi Polyporus, Daedalia, Daldinia, and others (Stillwell 1960, 1964, Vaartaja and 

King 1964), the spores of which are transmitted by females during oviposition (Stillwell 1964). A dual 

effect of horntails on wood has been discovered. The horntails inoculate the tree with a special 

secretion which causes needle yellowing and weakening of tree resistance to fungi (Coutts 1969). 

Inoculation by the fungi causes changes in wood properties that facilitate tree occupation by horntails 

(Sinadsky 1967, Schimitschek 1974). On wood sections, the direct correlation between horntail attacks 

and fungus mycelium infections is vividly evident. 

Strong preference for wood infected by basidium fungi was also found in some Peltidae and 

Buprestidae species. Peltis grossum L. (European-West Siberian species) and P. giganteum Rtt. (East 

Siberian species) are typically found with the brown rots of conifers and Ostoma ferrugineum L. with 

the brown birch rots caused by the fungus Piptoporus betulinus. The larvae develop only in the wood 

infected by mycelium. The possibility of spore transmission by species of Peltidae has not yet been 

studied. 

Direct connections between damage to asian poplars Populus pruinosa, P. ariana, and other 

species by the popylore Inonotus pseudohispidus and the buprestid beetle Eurythyrea oxiana Sem. were 

recorded in the riparian forests of Middle Asia. Both the fungus and the beetle species are extremely 

common there. The fungus infects weakened, but visibly vigorous trees. The infected wood takes on a 

brownish or red color due to pigment accumulation (Sinadsky and Bondarceva 1956). The buprestid 

larvae occupy only those wood sections infected by the fungus. Conditions for spread of the fungus 

have not been studied. The spores are thought to penetrate to the wood at various injury sites 

(Sinadsky and Bondarceva 1956). At the same time, the close connections between the buprestid 

larvae and the fungus (common area, beetle habitation only in fungus-infected wood zones, initial 

occupation by both beetle and fungus of the trunk base) testify to the possibility of spore transmission 

by beetles. It is quite possible that the connections between this insect group and the fungi are not 

simple and belong to a different category of insect/fungal relationship. This supposition is confirmed 

by the example of the horntails, for many of which mutualistic, symbiotic relations are evident. Thus 

Xeris spectrum L. (Siricidae) with poorly developed mycetangia injure wood only during the year 

following occupation by another horntail species (Spradbery 1974), which infect it with fungi. 

Species Trophically Associated with Fungus-Infected Wood 

and Lacking Special Structures for Fungal Transmission 

This group includes the destructive xylophages breeding in light and brown wood rots. Wood 

occupation takes place quite long after fungi inoculation. The imago of this insect group tries to 

locate tree trunks suitable for colonization (Mamaev 1974c). By wood boring, xylophages promote 

various microorganisms and fungi activity (Callaham and Shifrine 1960, Mamaev 1960) and favor their 

penetration of the wood through galleries (Hesterberg et al. 1976). 

The capacity of this group to feed on poorly assimilated, less nutritional wood pulp in the 

absence of ectosymbiotic associations with fungi can be explained by the presence of cellulases in the 

intestine. So, unlike bark and capricorn beetles feeding on bark and sap-wood and possessing 

hemicellulase, the capricorns as typical inhabitants of destructive rots have a set of cellulases, 

promoting cellulose utilization by the insect (Chararas 1983, Chararas and Chipoulet 1983, Kukor and 

Martin 1986). The high cellulases concentration in the intestine is thought to result from fungi 

reproducing in the folds of the intestine (Schlottke 1948, Mamaev 1960, 1974c). At the same time, 

capricorn beetles breeding in weakened trunks on the border of xylem and phloem were discovered to 

possess an extra set of enzymes and yeast, favoring assimilation of the carbohydrates (Chararas and 

Pignal 1981 ). 

340 
Brown rots most often form under the influence of the polypore Fomitopsis pinicola and are 

most common to conifers. The typical inhabitants of brown wood rots in the European part of the 

U.S.S.R. are Toxotus cursor L (Cerambycidae), Ceruchus chrysomelinus Hochw., and Aesalus scarabeoides 

Pz. (Lucanidae ). In the mountains of the Caucasus, the last of these species is replaced by Aesallus 

ulanovskyii Gglb. (Kosarjevskaya and Mamaev 1962, Mamaev 1977). 

The typical destroyers of brown rot wood in the Far East are the cockroach, Cryptocercus relictus 

B. Bien., the beetles Prostomis mordox Rtt. (Cucujidae), Istrisia rufobrunnea Lew. (Salpingidae), 

Nematoplus semenovi Nik. (Nematoplidae ), Phellopsis amurensis Heyd. (Zopheridae ), and others 

(Mamaev 1973a, 1973b, 1974b). Among Diptera, the most common inhabitant of brown rots is 

Hyperoscelis eximia Bohem. (Canthyscelidae). 

The light rots, usually developing under the influence of the tinder fungus Fomes fomentarius, 

are most typical to leaf-bearing trees. The light rot wood in the European part of the U.S.S.R. are 

usually destroyed by the larvae of common stag beetles, Lucanus cervus L., Dorcus parallelopipedus L, 

and Sinodendron cylindricum L (Lucanidae), and the larvae of dipterans, Tanyptera atrata L., Dictenidia 

bimaculata L (Tipulidae ), and Epiphragma ocellaris L (Limoniidae ). The main consumers of light rots 

in the Far East are the stag beetles, Prismognathus subaeneus Motsch. and Eurytrachelus rubrofemoratus 

Voll. (Lucanidae ), the darkling beetles, Misolampidius tentyrioides Sols (Tenebrionidae ), and the 

dipterans, Phoroctenia vittata Mg., Tanyptera nigricomis Mg. (Tipulidae), Hesperinus rohdendorji Kriv. et 

Mam. (Hesperinidae ), and Pachyneura oculata Kriv. et Mam. (Pachyneuridae ). In this group one can 

also find the beetles Melandrya mongolica Motsch. (Melandryidae) and Dentisca serridens Ter.-Min. 

(Curculionidae ). 

Among the ecological groups considered, two groups of destroyers (bark and capricorn beetles) 

can be classified as xylophages, and the last homtails, peltids, and some buprestids as xylomycetophages, 

because of their feeding on wood infected by fungus mycelium. 

CONCLUSIONS 

Vigorous trees have diverse properties for facilitating their resistance against consumers. 

Moreover, wood is a substance resistant to degradation. Therefore, representatives of the 

"tree-fungus-insect" system have evolved allowing insects to exploit a vast resource. 

My attempt to classify these relations is no doubt far from being complete, partly because the 

delicate mechanisms of insect-fungi interactions have as yet been insufficiently studied. Nevertheless, 

the examples presented permit us to conclude that complicated insect-fungi relationships exist at all 

successional stages of wood degradation (Lindemann 1986). 

SUMMARY 

Based on the forms of their interrelationships with fungi, we distinguished four groups of 

insects: 1) ambrosia mycetophagous insects, symbiotically associated with primary ambrosia fungi; 

2) ambrosia xylomycetophagous (phloeomycetophagous) insects, symbiotically associated with 

wood-coloring fungi; 3) xylophagous insects, symbiotically associated with vascular mycosis fungi; and 

4) destructive xylo-, mycetophagous insects, associated with wood-destroying fungi. Among the 

destructive xylo-, mycetophagous insects, three ecological subgroups were identified in terms of their 

trophic and symbiotic connections with fungi. 

341 
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344 
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345 
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346 
ON THE ROLE OF THE TREE 

IN RELATION TO COLONIZATION 

BY IPS TYPOGRAPHUS L. 

S. BOMBOSCH 

Institut ftir Forstzoologie der Universitlt GOttingen 

Busgenweg 3 

D-3400 GOttingen, Germany 

INTRODUCTION 

For roughly 200 years it was assumed that trap trees attracted the bark beetle Ips typographus by 

means of specific chemical compounds produced by the tree. After the aggregation pheromone was 

discovered, the importance of tree volatiles was at first more or less totally denied (Vite 1980). 

Since Johann succeeded in proving that the combination of pheromone plus tree is, at times, 

considerably more attractive than the combination of Pheroprax plus plastic trap (Bombosch et al. 

1982, Johann 1986a, 1986b ), more attention has been paid to the tree even by pheromone supporters 

(Bakke 1985, Vite and Franke 1985). What follows is a brief synopsis of the findings thus far obtained 

on this question at our institute. 

FLIGHT--A FUNCTION OF ENERGY RESERVES 

After leaving their breeding tree or winter quarters, by no means all beetles react immediately to 

stimuli from trees or pheromones. A large proportion, on the contrary, fly directly from the forest 

surroundings into the bright sky. According to investigations by Botterweg (1982) and Gries (1985), 

the proportion of the total population made up of these migrating beetles and the length of the 

migratory phase of individual beetles depends on the individual beetles' energy reserves. These are 

determined earlier by the amount of nourishment at the larvae's disposal. The model calculations of 

DeJong and Saarenmaa (1985) were very successful in showing these shifts in the nutritional condition 

of individuals in a population. 

These findings allow us to see that an L typographus population contains at least two different 

groups of individuals: one which migrates and one which does not. The proportion of these two 

groups is not constant since the population density of the larvae, which is determinant here, depends 

upon the respective breeding trees available. 

VERTICAL SILHOUETTES AND VOLATILES 

Let us track the course of the migrating beetles. Their flight into the bright light brings about 

a great dispersion as a result of which, in addition to a high mortality rate, we can find L typographus 

everywhere in the countryside (Bakke 1985, Sanders 1984, Gossenauer 1988). Their distribution is not 

BARANCHIKOV, Y.N., MATrSON, W.J., RAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

347 
uniform, however. The lowest densities are to be found in agricultural areas and in very dense young 

deciduous forest stands; conifer cultures are also less often visited than older deciduous stands. This 

indicates that both the vertical silhouette of the trees and the scents specific to spruce are important 

to the beetles after their migratory flight. This behavior leads to a more concentrated occurrence in 

spruce stands but also to the beetles' marked presence in deciduous stands. For this reason, according 

to our calculations, it is not possible to reduce population density with the help of traps (Table 1) 

(Bombosch in press). Gries et al. (1989) maintain that L typographus would have no chance of survival 

if it were to find its breeding trees only by accident. As a lone insect, furthermore, it is not in a 

position to successfully colonize healthy spruce trees. This migratory portion of the beetle population, 

operating on its own, is dependent upon suitable fallen or standing stems. The silhouette and the 

odoriferous quality of the tree itself probably combine to help the beetles find such stems. All earlier 

attempts to increase the efficiency of trap trees, as recorded in the textbooks, point in this direction. 

To date, as far as I know, it has not been possible to analyze the chemical structure of the odoriferous 

substances produced by the tree. It is very unlikely that a-pinene alone is the attractive substance 

(Vite 1980) because if that were the case all conifers would be colonized. After the beetles have 

penetrated the bark, the attractiveness of the trees attacked is intensified by the secretion of 

pheromone. Genuine pioneer beetles initiate this process; every additional beetle that is attracted and 

produces pheromone in its tum increases the allure of the potential breeding place. In tests with the 

method developed by Dedek and Pape (1988a, 1988b) of applying methamidophos as an insecticide that 

takes effect only in the bark, it was noted that the beetle infestation on standing trees was 

concentrated at a few meters surrounding the pheromone dispenser, whereas beetles appear to colonize 

the entire length of fallen trees. After landing, then, these beetles seem to spread more intensively in 

a horizontal direction than vertically. 

Numerous other species besides L typographus colonize fallen spruce stems. According to Vite 

and Franke (1985), the range of species on these trees is determined by the types of change that occur 

in the bark. A dry change leads to colonization by L typographus, L amitinus, P. chalcographus. A wet 

change, whereby ethanol is released, is responsible for colonization by Xylosandrus germanus and 

Trypodendron sp. etc. Within these groups, diverging pheromones are suspected (Vite and Franke 

1985) of causing the delimitation of the individual species' territories. In spring 1989 L typographus, 

L amitinus, P. chalcographus, and P. polygraphus, and also T. lineatum were found in very close 

proximity to each other on 3-m-long lower stem sections in the Soiling hills. 

TEMPERATURE EFFECfS ON FLIGHT 

The demands, at least of the teetotallers, seem therefore to cover a very large range, and the 

importance of the deflecting pheromones is not exactly paramount. In my opinion, when trying to find 

out the causes for the different species' distribution on the stem, more attention should be directed to 

the temperature necessary for setting them into flight than has hitherto been paid. In 1987 we were 

able initially to observe a strong flight of L amitinus in two low mountain ranges. When L typographus 

flew 3 weeks later after a sudden onset of cold weather, it was able to colonize only those places that 

had been left open by its predecessor. It is thus quite conceivable that an exact spatial separation of 

the individual species occurs according to temperature thresholds when the temperatures rise slowly in 

spring, but that the commingling described above occurs when the temperature suddenly turns hot, 

using all species' thresholds. 

348 
Table 1. Calculation of the reduction of the population of Ips typographus by 

different success of trapping 

Spruce Spruce 

clearcuts stands Total Reduction 

Parameter 10 ha 90 ha population rate % 

Distribution {Johann, 

Gossenauer) 20% 80% 

Assumed populationfha 200 800 

Total 2,000 72,000 74,000 

Reduction on clearcuts 

Johann, Beuke {-17%) -340 72,000 73,680 0.4 

Weslien {-30%) -600 72,000 73,400 0.8 

Hypothetical {-50%) -1,000 72,000 73,000 1.3 

Assumed population {Bakke) 6,000 68,000 74,000 

Reduction on clearcuts 

Johann, Bueke {-17%) -1,020 68,000 72,980 1.4 

Weslien {-30%) -1,800 68,000 72,200 2.4 

Hypothetical {-50%) -3,000 68,000 71,000 4.0 

Hypothetical {-100%) -6,000 68,000 68,000 8.1 

TEMPERATURE AND LIGHT EFFECfS ON PIONEERS 

In contrast to fallen trees, healthy, standing stems cannot be colonized by single beetles since for 

that a simultaneous attack by many individuals is necessary. Aggregation is supposed to materialize as 

single, pioneer beetles land on the tree and then attract more and more beetles by the production of 

contact pheromone, until finally the number of insects necessary for a successful attack is present (Vite 

1980). This hypothesis assumes that beetles, having once landed, do not fly ·away again, and leaves 

open the question by which criteria the first beetles choose their landing place and what it is that 

triggers the mass attack. 

Our observations suggest that pioneer beetles do not play a part in the colonization of standing 

trees. On standing spruce trees we have never as yet found increasing congregations before the beetles' 

penetration. On the contrary, in the spring of 1989 we found, apart from numerous stem sections on 

the ground that had been attacked, single standing trees exhibiting "Spechtspiegel" on the lower part of 

their stems. Spechtspiegel are small pale patches appearing on the bark where the squamae have been 

removed by woodpeckers or other birds in search of xylophages. We also found one tree with ten, and 

three trees each with one, unsuccessful boring attempt. This indicates that the bulk of the insects in 

the L typographus population we observed was searching for wood lying on the ground, but that a few 

individual insects reacted to standing trees and attempted to attack them (e.g. the Spechtspiegel). An 

attack on standing trees does not, therefore, require presence of many beetles reacting in the same way. 

It was also evident that Spechtspiegel and boring attempts did not occur at random around the stems, 

but always faced south to southwest. This observation accords with the long known fact that when 

standing trees are attacked, mass propagation in a beetle "nest" is usually to be found where the sun 

349 
shines in the afternoon. As the triggering stimulus for beetles in search of suitable standing wood, 

differences in the trees' warmth may be of more decisive importance than their scents. The number of 

beetles attacking, however would not depend on the strength of the allurement, but on the number of 

beetles reacting to particular degrees of warmth of the trees. These may represent the nonmigratory 

portion of the population mentioned earlier. The fact that an attack on a standing tree always occurs 

in the immediate vicinity of an earlier attack in a beetle nest speaks in favor of this hypothesis. It can 

also be observed that the infestation of wood lying on the ground subsides in the course of a gradation 

(Bombosch 1954). This may be the result of a deterioration in the larvae's nutrition due to increasing 

population density together with a simultaneous reduction of breeding possibilities causing a continuous 

reduction in the number of migrating individuals. Since the relationship between the number of 

beetles and suitable breeding places is not constant, the question why each blowdown that is colonized 

by L typographus does not endanger neighboring stems can still be answered. But the question to what 

extent this part of the beetle population reacts to pheromone traps still remains completely open. The 

investigations begun by Sahota and Peet (1988), whose objective is to characterize the quality of bark 

beetle populations, should contribute to considerable progress in the elucidation of this complex of 

questions. 

SUMMARY 

When assessing L typographus populations, one should differentiate between the proportion of 

migratory and nonmigratory individuals. The reason for this difference may be found in changes in the 

larvae's nutrition. Individuals in the migratory proportion set off alone and are dependent on finding 

suitable stems. They search for them purposefully, probably because of the silhouette and primary 

attractive substances of these trees. The first to colonize intensify the tree's allurement by pheromone 

secretion. They are genuine pioneer beetles. 

With respect to breeding suitability of the tree, the beetles' requirements do not seem to be as 

restrictive as has hitherto been assumed, since L typographus and T. lineatum can be found next to each 

other on the same stem. As for spatial distribution of the individual species on the stem, not only 

deflecting pheromones but also the temperature conditions and differences in the beginning of the 

flying period of the individual species should be considered. In beetle nests, the attack of standing 

trees may be caused by the nonmigratory portion of the beetle population. Temperature differences 

between the trees may function as directing stimuli. A mass attack would not be determined by 

intensity of the allurement, but by the number of nonmigratory beetles in the given population. 

LITERATURE CITED 

BAKKE, A 1985. Deploying pheromone-baited traps for monitoring Ips typographus populations. 

Z ang. Ent. 99: 33-39. 

BOMBOSCH, S. 1954. Zur Epidemiologie des Buchdruckers (Ips typographus L), p. 239-283. In 

Wellenstein, G. Die grosse Borkenldiferkalamit!t in Siidwestdeutschland 1944-1951. Selbstverlag, 

Ulm. 

BOMBOSCH, S. 1989. Possibilities and limits for the use of pheromone traps against Ips typographus 

L Proc. Symp. EPS IOBC Borjomi, Sept. 1989 (in press). 

BOMBOSCH, S., JOHANN, M., and RAMISCH, H. 1982. Versuche zur Verbesserung der 

Fangergebnisse von Borkenldifem. Holzzentralblatt 129: 1852-1853. 

BOTIERWEG, P.F. 1982. Dispersal and flight behavior of the spruce bark beetle Ips typographus L in 

relation to sex, size and fat content. Z ang. Ent. 94: 466-489. 

350 
DEDEK, W. and P APE, J. 1988a. Integrated pest control in forest management--combined use of 

pheromones and insecticides for attracting and killing the bark beetle Ips typographus. I. Studies 

with 32P-labelled methamidophos in the ascending sap of spruce. For. Ecol. Manage. 26: 47-61. 

DEDEK, W., P APE, J., GRIMMER, F., and_ KORNER, H.-J. 1988b. Integrated pest control in forest 

management--combined use of pheromones and insecticides for attracting and killing the bark 

beetle Ips typographus. II. Effects of methamidophos treatment following bark penetration into 

the ascending sap of pheromone-baited spruce. For. Ecol. Manage. 26: 63-76. 

DEJONG, M.E.M. and SAARENMAA, H. 1985. A mechanistic simulation model for the movement 

and competition of bark beetle larvae (Coleoptera, Scolytidae). Ecol. Model. 27: 109-139. 

GOSSENAUER, H. 1988. Untersuchungen zum Nachweis der Bedeutung prirrutrer Lockstoffe fiir die 

Anlockung des Buchdruckers Ips typographus L (Coleoptera: Scolytidae). Diss. Forstl. Fak. 

GOttingen. 

GRIES, G. 1985. Zur Frage der Dispersion des Buchdruckers (Ips typographus L.). Z ang. Ent. 

99: 12-20. 

GRIES, G., NOLTE, H., and SANDERS, W. 1989. Computer simulated host selection in Ips 

typographus. Entomol. Exp. Appl. 53: 211-217. 

JOHANN, M. 1986a. Zur Anlockung des Buchdruckers (Ips typographus L) 1. Die Lockwirkung 

naturlichen Brutmaterials. Z ang. Ent. 101: 332-342. 

JOHANN, M. 1986b. Zur Anlockung des Buchdruckers (Ips typographus L) 2. MOglichkeiten der 

Integration naturlichen Brutmaterials in die Beldtmpfung mit Pheromone. Z ang. Ent. 

102: 113-216. 

SAHOTA, T.S. and PEET, F.G. 1988. Changes in the quality of scolytid Populations: their 

determination and relation to scolytid outbreaks. Proc. IUFRO Work. Part. 17th Int. Congr. Ent. 

Symp. Integrated Control of Scolytid Bark Beetles. 4 July 1988. Vancouver, B.C. 

SANDERS, W. 1984. Ein Beitrag zum Verhalten des Buchdruckers Ips typographus L. wihrend der 

Flugphase. Anz. SchAdlingskd. 57: 131-134. 

VITE, J.P. 1980. Forschungsbericht 1980. Schwerpunkt: Borkenldtferpheromone. Freiburger 

Waldschutz-Abh. Bd. 3. 

VITE, J.P. and FRANKE, W. 1985. Waldschutz gegen Borkenldtfer: Vom Fangbaum zur Faile. 

Chem. unserer Zeit. 19: 11-21. 

351 
INTERSPECIFIC OLFACTORY COMMUNICATION 

IN THE SOUTHERN PINE BARK BEETLE GUILD1 

T.L. PAYNE,2 M.T. SMITH,3 M.C. BIRCH,4 and A ASCOLI2 

2Department of Entomology 

Virginia Polytechnic Institute and State University 

Blacksburg, VA 24061 U.S.A 

3USDA-ARS 

P.O. Box 87 

Byron, GA 31008 U.S.A 

4Department of Zoology 

South Parks Road 

Oxford, OXl 3PS United Kingdom 

INTRODUCTION 

The southern pine bark beetle guild consists of many species, the most economically significant 

of which are the five scolytid species, Dendroctonus frontalis Zimmermann, D. terebrans (Olivier), Ips 

calligraphus (Germar), 1 avulsus (Eichhoff), and 1 grandicollis (Eichhoff). All five species co-exist in 

pine forests across the southern and southeastern United States. When the species cohabit in the same 

host tree each usually occupies a distinct niche. However, the area occupied by one species generally 

overlaps with that occupied by another (Fig. 1) (Birch and Svihra 1979, Dixon and Payne 1979, Birch 

et al. 1980, Svihra et al. 1980, Paine et al. 1981, Wagner et al. 1985. 

Host selection, aggregation and colonization by all the various species involves a complex 

chemical communication system composed of compounds produced both by the beetles and by the host 

tree. Electrophysiological investigations have shown that each species has antennal olfactory receptors 

capable of detecting semiochemicals produced by itself and by the other species in the guild (Payne 

1970, 1971, 1974, 1975, Payne and Dickens 1976, Dickens and Payne 1977, Payne et al. 1982, 1987, 

1988, Smith et al. 1988). Behavioral investigations of some of the species have shown that they 

respond to intra- and interspecific semiochemicals, as well as to volatiles from beetle-infested host 

materials (Renwick and Vite 1969, Werner 1972, Hedden et al. 1976, Payne et al. 1978, Richerson and 

Payne 1979, Dixon and Payne 1980, Billings 1985, Siegfried et al. 1986, Payne et al. 1987, Payne et al. 

1988, and Phillips et al. 1989). Investigations have also shown the response patterns of the ·species to 

1Research supported in part by CSRS Grant #86-CRCR-1-2270, NATO Grant 

#CRG.0710/86, and Texas Agricultural Experiment Station project MS1525 (while 

M.T. Smith and T.L. Payne were with Texas A&M University). The findings, 

opinions, and recommendations expressed herein are those of the authors and 

not necessarily those of the U.S. Department of Agriculture. 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

352 
trees or logs containing the various members of the guild (Vite et al. 1964, Godbee and Franklin 1976, 

Birch et al. 1980, Svihra et al. 1980, Svihra 1982, Phillips et al. 1989). In this paper, using both new 

findings and previously published information, we survey the interspecific olfactory receptor sensitivity 

of the species for specific pheromones and explore the behavioral responses of the most significant 

species in the southern pine bark beetle guild to the pheromonal blends of the species. 

EXPERIMENTAL METHODS 

Antenna! olfactory responses were measured using the electroantennogram (BAG) and singlecell techniques (Schneider 1957; Boeckh 1962, Payne 1975, Dickens and Payne 1977). BAGs were 

recorded with glass capillary, Ag-AgCl microelectrodes filled with 3M KCI. The recording electrode 

was inserted in the antenna! club, and the indifferent electrode was inserted in the beetle's head 

capsule or mouth. Single-cell recordings (SCR) were made using tungsten electrodes with 

electrolytically polished tips of < 2 u. The recording electrode was inserted at the base of a sensillum 

in the sensory bands of the antenna; the indifferent electrode was inserted in the mouth. Responses 

were recorded on magnetic tape and polaroid film. The compounds tested, their source, and their 

purity are given in Table 1. Test stimuli were delivered as 5 ul aliquots onto a piece of filter paper in 

a glass cartridge via a 1 Umin airflow. Serial dilutions of the stimuli were presented in order from 

the lowest to the highest concentration. Dosage-response curves plotted from mean responses to each 

stimuli were used to determine the relative sensitivity of the olfactory receptors to each compound. 

The threshold of response, the minimal stimulus concentration at which an BAG was detectable above 

background, was considered an indication of olfactory receptor sensitivity to a compound. 

Table 1. Beetle- and host-tree-produced compounds tested 

Compound Source of supply Purity (%) 

Frontal in 

(+,-) Chern. Samp. Co. 99 

(+) K. Mori 98 

(-) K. Mori 98 

Verbenone 

(+,-) Chern. Samp. Co. 98 

(+) Chern. Samp. Co. 98 

(-) Chern. Samp. Co. 98 

endo-brevicomin Chern. Samp. Co. 99 

Ipsdienol Borregaard Industries 81 

Ipsenol Borregaard Industries 89 

cis-verbenol Borregaard Industries 95 

tra.ns-verbenol Borregaard Industries 95 

a-pinene Aldrich Chern. Co. 97 

353 
--, I 

I 

I 

I 

I 

I I __ ..J ..J 

-, 

I 

I 

I 

~ I. avulsus 

I. 

~ grandlcollis 

i~ 1. calligraphus 

D. ~ frontalis 

D. terebrans 

Figure 1. Primary species of the southern pine bark beetle guild and their 

generalized spatial distribution on the host tree. (From Flamm et al. 1988.) 

Our field studies were conducted in the east Texas pine forest during the summer of 1987. To 

minimize possible effects of host ·tree odors on beetle response, the studies were carried out in a 

2-year-old clear-cut. The surrounding forest was mostly loblolly pine, Pinus taeda, and, to the best of 

our knowledge, no bark beetle infestations were present within ca. a 50-mile radius. At the time, 

beetle populations in Texas were considered to be at an endemic level. As a result, the number of 

beetles trapped during the study was low. 

Test Compounds 

Pheromonal blends for the guild members were determined from published and unpublished 

reports of pheromone production and were individually formulated and tested. In addition, specific 

enantiomers of the major pheromonal components were evaluated for D. frontalis and the Ips spp., 

since previous research had demonstrated differential production and/or responsiveness based on 

enantiomeric composition (see references, Table 2). To determine the presence and relative abundance 

of flying beetles of each species in the test area, a Dendroctonus standard composed of frontalin and 

turpentine and an Ips standard composed of ipsdienol, ipsenol, and cis-verbenol (Billings 1985) were 

included as separate treatments in the experiments. A trap baited only with turpentine and a blank 

trap were included as controls for response to host odor and trap configuration, respectively. 

354 
Table 2. Beetle-produced pheromonal blends tested 

[1] [ 2] Elution rate [3] 

Species Sex Chemical compounds Compound ratios (mg/24 h) Reference 

D. frontalis F (-) -F: (+) -F:TV:V 21.25:3.75:750:6 0.85:0.15:30:0.24 1,2 

D. frontalis M (+)-ENB:(-)-ENB:EXB:V:TV 0.94:0.03:0.03:800:9 0.94:0.03:L0.03:800:9 2,3 

D. terebrans F F:TV:V 1:500:50 1:500:50 2,4 

M EXB:TV:V 1:15:1.1 1:15:1.1 2,4 

I. calligraphus M (R)-(-)-,(~)-(+)-IPSD:TV:CV 2:2.5:1 0.2:0.25:0.1 5,6 

M (R)-(-)-IPSD:TV:CV 2:2.5:1 0.2:0.25:0.1 6 

M (~)-(+)-IPSD:TV:CV 2:2.5:1 0.2:0.25:0.1 6 

~I. calligraphus F TV:CV 5.5:1 4.4:0.8 5 

VI 

I. avulsus M (R)-(-)-,(~)-(+)-IPSD:TV:CV 45:1:1 0.2:0.0044 5,6 

M (R)-(-)-IPSD:TV:CV 45:1:1 0.2:0.0044 6 

M (~)-(+)-IPSD:TV:CV 45:1:1 0.2:0.0044 6 

I. grandicollis M (~)-(-)-,(R)-(+)-IPSE:TV:CV 73:1:1 0.2:0.0027:0.0027 5,7 

(~)-(-)-IPSE:TV:CV 73:1:1 0.2:0.0027:0.0027 7 

(R)-(+)-IPSE:TV:CV 73:1:1 0.2:0.0027:0.0027 7 

[1] Sex: F - female; M - male. 

[2] CV - cis-verbenol, ENB - endo-brevicomin, EXB - exo-brevicomin, F- frontalin, IPSO - ipsdienol, IPSE -

ipsenol, TV = trans-verbenol, and V - verbenone. 

[3] 1) Stewart et al. 1977, 2) Payne, West, Silverstein (unpubl.), 3) Redlich et al. 1987, 4) Payne et al. 

1987, 5) Vite et al. 1972, 6) Vite et al. 1978, and 7) Vite et al. 1976. 
Elution Devices and Rates 

Based on weight loss/24 h, elution devices were developed and rates determined for each 

compound tested (Table 2). Glass capillaries and vials of various sizes provided the desired elution 

rates. 

Experimental Design 

The multiple funnel trap was used to monitor the beetles' response to the different pheromonal 

blends (Lindgren 1983). Traps were placed ca. 45 m apart in a single, straight row running through 

the center of the clear-cut. Initially, treatments were assigned positions randomly. Thereafter, 

treatments were advanced one position each subsequent day in order to minimize positional effects and 

disproportionate trap catches caused by any nonrandom distribution of beetles. Thus each treatment 

occupied each position during the 20-day experiment. Every 24 h, trapped beetles were removed and 

placed in labeled vials for subsequent counting and sexing. Chi Square and/or Fisher's exact tests were 

used to analyze the data, followed by a binomial test for paired comparisons, when appropriate (Sokal 

and Rohlf 1981 ). 

RESULTS AND DISCUSSION 

Olfactory Perception 

Electroantennogram analyses of the species have consistently shown that each species possesses 

more receptors with lower thresholds for compounds produced by conspecifics and to which they are 

behaviorally most responsive (Payne 1970, 1971, 1974, Dickens and Payne 1977, Payne et al. 1982, 1988, 

Smith et al. 1988). For examples, see Figs. 2 and 3. 

More detailed investigations of the peripheral olfactory receptor systems have been made using 

single cell recording (SCR) techniques (Fig. 4). 

Both general and chiral-specific acceptors have been identified, as well as a wide variety of 

olfactory cell types with different degrees of receptor specificities which range along a continuum from 

cells narrowly tuned to a single compound to cells broadly tuned to a number of different compounds 

(Figs. 5-7). 

Compounds which attract and/or arrest, enhance attraction or reduce attraction, may be 

perceived by a common neuron and acceptor. These overlapping acceptor specificities may provide the 

beetles with the genetic plasticity needed to code both qualitative and quantitative information about 

several behaviorally significant odors present in the insects' environment. 

Behavioral Response 

The responses of D. frontalis, D. terebrans, L calligraphus, L avulsus, and L gran.dicollis to the 

Dendroctonus and Ips standards (treatments 17 and 18) verified that the species were present 

throughout the test area for the duration of the experiment, even though, due to their endemic 

population levels, the number of beetles trapped was low. 

D. frontalis 

As expected, both male and female D. frontalis were attracted to the pheromonal blends of 

female D. frontalis and, to a lesser extent, female D. terebrans (treatments 1 and 4) (Fig. 8). Attraction 

to both blends can be attributed to the presence of frontalin and trans-verbenol. D. frontalis has been 

356 
200 

~ 8.150 

; 

Q:: 

~100 U.l 

ee 

6 

Q) 50 

::E 

0 ipsdienol 

·5 -4 -3 ·2 ·1 0 1 2 

Sx Jog 10ug 

d Ipsen of 

-5 ..4 -3 ·2 -1 0 1 2 

Sx log 10ug 

g (±)-frontalin 

·S -4 ·3 ·2 ·1 0 1 2 

Sx log 10ug 

<:!:)-verbenone 

-5 ..4 ·3 -2 -1 0 1 2 

Sx log 10ug 

200 

Q) 

~ 

~150 

Q) 

Q:: 

~100 U.l 

~ 

~ so ~ 

200 

CD 

~ 

8_150 

; 

Q:: 

~ 100 U.l 

ee 

6 

Q) 50 

~ 

200 

Q) 

~ 

~ 150 

& 

~ 100 1.1.1 

~ 

c 

0 

Q) 50 

~ 

b cis-verbenol 

-5 ..4 -3 ·2 -1 0 1 2 

Sx log 10ug 

-5 o4 ·3 ·2 ·1 0 1 2 

Sx log 10ug 

h (+)-frontafin 

·5 -4 ·3 ·2 • 1 0 1 2 

Sx log 10ug 

k ®·< + >-verbenone 

·5 ·4 ·3 ·2 ·1 0 1 2 

5xlog10ug 

CD 

~ 

8_150 

... 

g_ 

~ 10 U.l 

~ 

6 

CD 

~ 

200 

~ 8.150 

... 

CD 

Q: 

~ 100 U.l 

~ 

6 

Q) 50 

~ 

200 

CD 

~ 0 150 '* CD 

Q: 

~ 100 1.1.1 

~ 

c 

0 

Q) 50 

~ 

200 

~ c 

~150 

& 

~ 100 U.l 

~ 

~ 50 

~ 

C trans- verbenol 

·5 -4 ·3 ·2 ·1 0 1 2 

Sxlog lOug 

f endo -brevicomin 

·5 -4 ·3 ·2 ·1 0 1 2 

Sxlog lOug 

(-)-frontalin 

·5 -4 ·3 ·2 ·1 0 1 2 

Sxlog lOug 

I ~-( • )·verbe none 

·5 -4 ·3 ·2 ·1 0 1 2 

5 x log lOug 

Figure 2. Mean percentage response of I. avulsus, I. calligraphus, and 

I. grandicollis to behavioral chemicals. Means are percentage of EAG to the 

standard ipsdienol. o- I. avulsus; •- I. calligraphus; ~-I. grandicollis. 

(From Smith et al. 1988.) 

357 
,...... 300 

w 

(,f) 

+I 

....... 

"2 250 

a 

"E 

.2 

(,f) 200 

.£ Dendroctonus terebrons 

Q) 

~ -a 150 II male 

Q) II c: female 

~ 

~ 100 

ae 

E 50 ;:::, 

E 

x 

a 

2 

0 

1 2 3 4 

Compound 

Figure 3. Maximal percentage of EAGs to behavioral chemicals recorded from 

male and female Dendroctonus terebrans N - 5; vertical bars represent ± x SE. 

Standard = 5 ug frontalin. 1 - Frontalin, 2 - endo-brevicomin, 3 - transverbenol, 4- turpentine. (From Payne et al. 1987.) 

reported to be attracted to frontalin and frontalin plus trans-verbenol (Renwick 1969, Renwick and 

Vite 1969, 1970, Payne et aL 1978, Billings 1985). Trans-verbenol has been reported significantly to 

enhance the attraction of D. frontalis to frontalin (Renwick 1969, Renwick and Vite 1970, Payne et al. 

1978). 

Male and female D. frontalis were not attracted to the pheromonal blends of male D. frontalis 

(treatment 2) or male D. terebrans (treatment 5). Responses of both sexes of D. frontalis to the 

pheromonal blend of female D. frontalis was significantly (P < 0.05) reduced by the simultaneous 

presence of the male D. frontalis blend (treatment 3). In part, these results can be attributed to the 

relatively high proportion of verbenone eluted from the blends of both male D. frontalis and male 

D. terebrans. Eluted at relatively high rates, verbenone has been reported to reduce D. frontalis 

attraction to frontalin plus a-pinene and/or trans-verbenol and frontalin plus turpentine (Renwick and 

Vite 1969, Payne et al. 1978). The results can also be attributed to the presence of ero-brevicomin, 

eluted from the blend of male D. terebrans, and ero-brevicomin plus endo-brevicomin, eluted from the 

blend of male D. frontalis. The brevicomins reduce D. frontalis attraction to frontalin plus a-pinene 

(Vite and Renwick 1971a, Payne et al. 1978). D. frontalis attraction to frontalin plus turpentine, with 

and without trans-verbenol, has also been reported to be reduced by endo-brevicomin (Payne et al. 

1978). More specifically, Vite et al. (1985) reported that (-)-endo-brevicomin significantly reduced 

D. frontalis attraction to frontalure (1:2 ratio of frontalin and a-pinene) plus turpentine. 

358 
frontal in 

:..:._!!~ 

A l 

verbenone 

;~ i I '~~~~~,~~-1~MtJ·!~~·~ 'f +t~~# ----------------------------------~~ 

ex-pinene 

1• 1H ~~~~~~~~~ 

3-carene 

•a t -l ·~~- ~· • 11 ~ J 1•1 tnt 4-rc lf t'-f ... 

Figure 4. Single-cell response from a sensillum basiconicum of a D. frontalis 

female to pheromones and host tree terpenes. Displaced horizontal bar 

(indicated by arrows) represents 1 sec stimulation. Delay from stimulus onset 

to spike initiation was due to an artifact in delivery system. (From Dickens 

and Payne 1978.) 

None of the pheromonal blends of the Ips species was attractive to D. frontalis (treatments 

7-16). The results correspond to the report by Billings (1985) of the lack of attraction of D. frontalis 

to an Ips pheromone blend, a mixture of 2 percent cis-verbenol, 2 percent ipsenol, and 2 percent 

ipsdienol in a vaseline-based paste, with and without turpentine. In addition, studies using beetleinfested pine bolts provided no evidence for the attraction of D. frontalis to bolts infested with 

L calligraphus, L avulsus, or L grandicollis (Vite et al. 1964, Birch and Svihra 1979, Birch et al. 1980, 

Svihra et al. 1980, Svihra 1982). 

359 
80 

60 

40 

20 

Females (n=74) 

i 0 c 

8. 80 Ul 

~ 

~ 

60 

Males (n=44) 

1 2 3 4 5 6 7 8 9 10 ,, 

Stimulus 

Figure 5. Percentage of Ips grandicollis olfactory cells which responded to 

stimuli. Shaded area equals percentage of cells which responded to only one 

compound. 1) spontaneous activity, 2) air, 3) pentane, 4) a-pinene, 

5) frontalin, 6) endo-brevicomin, 7) trans-verbenol, 8) cis-verbenol, 

9) verbenone, 10) ipsdienol, and 11) ipsenol. 

D. terebrans 

D. terebrans were trapped in such low numbers that analysis of their cross-attraction was not 

possible (Fig. 9). It should be noted, however, that the lack of response of D. terebrans to frontalin, 

frontalure, and trans-verbenol, separately, has been reported (Payne et al. 1987, Phillips et al. 1989). In 

combination with a high elution rate of turpentine, the pheromones were significantly attractive to 

360 
Stimulus Cell Type Stimulus Cell Type 

Compound A B c D E Compound E 

l] rn • frontalin • frontalin (+,-) 

trans-verbenol -I • frontalin ( +) 

cis-verbenol frontalin (-) Ill 

endo-brevicomin Bl rs:s trans-verbenol (+,-) II 

exo-brevi co min I trans-verbenol ( +) ... 

verbenone ~ - trans-verbenol (-) 

alpha-pinene • I alpha-pinene(+,-) 

ips enol ~ alpha-pinene ( +) I'RI 

ipsdienol f\'S! alpha-pinene (-) • 

Figure 6. Relative frequency of Figure 7. Relative frequency of 

nerve spikes from D. frontalis nerve spikes from a single D. 

olfactory cells in response to frontalis olfactory cell in response 

semiochemicals. to semiochemicals and enantiomers. 

D. terebrans, which indicates the presence of pheromonal-based interspecific communication between 

D. terebrans and D. frontalis, as reported earlier (Payne et al. 1987). 

L calligraphus 

Male and female L calligraphus were attracted to the pheromonal blends of male L calligraphus 

and L avulsus containing either racemic ipsdienol (treatments 7 and 11) or @)-(-)-ipsdienol (treatments 

8 and 12) (Fig. 10). More L calligraphus (P > 0.05) were attracted to the male L calligraphus blend 

containing racemic ipsdienol (treatment 7) than to the blend containing @)-(-)-ipsdienol (treatment 8). 

But L calligraphus were not attracted to the blends of male L calligraphus or male L avulsus containing 

@)-( + )-ipsdienol (treatments 9 and 13). Our results agree with earlier reports of the attraction of 

L calligraphus to ipsdienol plus cis-verbenol and ipsdienol plus trans-verbenol (Renwick and Vite 1972). 

361 
1.2 

~ 1.0 

Q 

..... 

~ 

~ 0.8 "- 2 

a. 

0 

u 

fh 

Q) 0.6 += 

Q) 

~ 

-

w 

(/) 0.4 

+I 

-c 

~ 0.2 ~ 

0.0 

Dendroctonus frontalis 

• male 

fZJ female 

1 2 3 4 5 6 7 8 9 1011 1213 14 1516 

a Treatment 

4 

3 

2 

0 

17181920 

Figure 8. Mean number of Dendroctonus frontalis trapped in response to 

pheromonal compounds eluted at varying rates. •see Table 2. Vertical bars 

represent standard errors of means. 

1) (-)-F:(+)-F:TV:V, 2) (+)-ENB:(-)-ENB:EXB:V:TV, 3) 1+2, 4) F:TV:V, 

5) EXB:TV:V, 6) 4+5, 7) (R)-(-)-,(~)-(+)-IPSD:TV:CV, 8) (R)-(-)-IPSD:TV:CV, 

9) (~)-(+)-IPSD:TV:CV, 10) TV:CV, 11) (R)-(-)-,(~)-(+)-IPSD:TV:CV, 12) (R)-(-

)-IPSD:TV:CV, 13) (~)-(+)-IPSD:TV:CV, 14) (~)-(-)-,(R)-(+)-IPSE:TV:CV, 

15) (~)-(-)-IPSE:TV:CV, 16) (R)-(+)-IPSE:TV:CV, 17) Dendroctonus standard, 

18) Ips standard, 19) turpentine standard, and 20) unbaited blank trap. 

More specifically, the results are in agreement with the report that for L calligraphus @-(-)-ipsdienol 

plus cis-verbenol was attractive, whereas (~)-( + )-ipsdienol plus cis-verbenol was not (Vite et al. 1978). 

However, the results reported here are not consistent with the report by Vite et al. (1978) that 

(~)~( + )-ipsdienol significantly reduced the attraction of L calligraphus to (R)-(-)-ipsdienol plus 

cis-verbenol. 

The pheromonal blends of male L grandicollis were not attractive to L calligraphus (treatments 

14-16). Although there are no reported analyses of the behavioral response of L calligraphus to the 

L grandicollis pheromone, ipsenol, when tested alone, the results presented here could be attributed to 

the lack of attraction of L calligraphus to ipsenol. By contrast, Birch et al. (1980) showed attraction of 

L calligraphus to L grandicollis-infested bolts; however, other researchers reported the lack of such 

attraction (Vite et al. 1964, Birch et al. 1980, Svihra 1982). 

The D. frontalis blends were not attractive to L calligraphus; for D. terebrans only the female 

blend exerted an attraction and that was slight. Dixon and Payne (1980) also reported the lack of 

362 
0.10 

0.16 

0.09 

8 Dendroctonus terebrans 0.14 

0.08 ~ 

8. 0.12 "0 0.07 ~ • male 

.2 II female 0. 0.06 0.10 0 

u 

~ 0.05 += 0.08 

J 0.04 

-

w 0.06 en 

+I - 0.03 

c 0.04 

j 0.02 

0.01 0.02 

0.00 0.00 

2 3 4 5 6 7 8 9 1 0 11 1213141516 17181920 

Treatment a 

Figure 9. Mean number of Dendroctonus terebrans trapped in response to 

pheromonal compounds eluted at varying rates. asee Figure 8. 

attraction of L calligraphus to frontalin, trans-verbenol, endo-brevicomin, exo-brevicomin, verbenone, and 

turpentine, when tested individually or in various combinations. Further, L calligraphus was reported to 

be unresponsive to D. frontalis-infested bolts (Vite et al. 1964, Birch et al. 1980, Svihra 1982). Dixon 

and Payne (1980), however, found that L calligraphus was attracted to bolts infested with female 

D. frontalis. 

L avulsus 

The pheromonal blends of male L calligraphus (treatments 7-9) and male L avulsus (treatments 

11-13) attracted both male and female L avulsus (Fig. 11). The blends of male L calligraphus 

containing racemic ipsdienol or (R)-(-)-ipsdienol (treatments 7 and 8) attracted significantly (P > 0.05) 

more L avulsus than the blend containing ~)-( + )-ipsdienol (treatment 9). Also, significantly 

(P > 0.05) more L avulsus were attracted to the blend of male L avulsus containing (R)-(-)-ipsdienol 

(treatment 12) than to the blend containing racemic ipsdienol (treatment 11). The blend of male 

L avulsus containing (R)-(-)-ipsdienol (treatment 12) was significantly (P > 0.05) more attractive to 

female than to male L avulsus. Our results are in agreement with those reported for the attraction of 

L avulsus to racemic ipsdienol and (R)-(-)-ipsdienol plus ~)-(-)-ipsenol (Hedden et al. 1976, Vite et al. 

1978). Furthermore, the results support reports of the attraction of L avulsus to male L avulsus--and 

to male L calligraphus-infested bolts (Vite et al. 1964, Birch et al. 1980, Svihra et al. 1980, Svihra 

1982). 

363 
. 0.80- 9.0 

> 0.70- 8.0 0 

Q Ips ca/1/graphus 

.... 

~ 0.60- • male 7.0 

~ ~ female 

:; 6.0 +-Q. 0.50-

0 ~ (!) ~ 5.0 (I) 

Q) ~ 0.40- += ~ Q) ~ 4.0 ~ ~ 

- 0.30- ~ w ~ ~ 3.0 (/) 

+I 

-c 0.20- ~ ~ 2.0 

~ ~ ~ 

~ ~ ~ ~ 0.10- ~ 

~ ~ ~ 1.0 

~ ~ . ~ ~ 

0.00 ~ ~ ~ 1/' 0.0 . . . 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 

Treatment a 

Figure 10. Mean number of Ips calligraphus trapped in response to pheromonal 

compounds eluted at varying rates. 8 See Figure 8. 

Few male L avulsus were attracted to the pheromone blend of male L grandicollis containing 

racemic ipsenol; females were not attracted. The results are supported by the reported attraction of 

L avulsus males over females to ipsenol (Hedden et al. 1976) and the attraction of L avulsus to male 

L grandicollis-infested pine bolts (Birch et al. 1980). Though not significant, L avulsus also showed 

some attraction to the blends of female and male plus female D. frontalis and D. terebrans (treatments 

1 and 3-6). While some studies have reported the lack of attraction of L avulsus to D. frontalisinfested bolts (Birch et al. 1980, Svihra 1982), others have demonstrated attraction (Vite et al. 1964, 

Svihra et al. 1980). It is apparent, however, that L avulsus is not strongly attracted to Dendroctonus 

pheromonal blends. 

L grandicollis 

Both sexes of L grandicollis were attracted to the pheromonal blend of male L grandicollis 

containing @)-(-)-ipsenol (treatment 15) (Fig. 12). The results support earlier reports that ipsenol 

(Vite and Renwick 1971b, Vite et al. 1976) and, more specifically, @)-(-)-ipsenol (Vite et al. 1976) are 

attractive to L grandicollis. The pheromone probably accounts in part for the attraction of 

L grandicollis to male L grandicollis-infested bolts, as reported earlier (Vite et al. 1964, Vite and 

Renwick 1971b, Birch and Svihra 1979, Birch et al. 1980, Svihra et al. 1980, Svihra 1982). (B)-(+)-

ipsenol was not attractive by itself (treatment 16), and significantly (P > 0.05) reduced attraction of 

L grandicollis to the male L grandicollis blend containing (~)-(-)ipsenol (treatment 14). The results 

agree with previous reports that (B)-(+ )-ipsenol significantly reduced the attraction of L grandicollis to 

(ID-(-)-ipsenol (Vite et al. 1976). The blends of male L grandicollis containing (ID-(-)-ipsenol attracted 

significantly (P > 0.05) more female than male L grandicollis (treatment 15). 

364 
1.0 

70 

0.9 

> 0 Ips avu/sus 

0 0.8 60 ~ • male s. 

"C 0.7 ~ fPJ female 50 

.2 

a. 0.6 0 

u 40 ~ 0.5 

~ 

~ 0.4 30 ,...... 

w 

tJ) 

+I 0.3 20 ~ 

c 

0 0.2 ~ 10 

0.1 

0.0 . 0 

1 2 3 4 5 6 7 8 9 1 0 11 1213141516 17181920 

Treatment a 

Figure 11. Mean number of Ips avulsus trapped in response to pheromonal 

compounds eluted at varying rates. 8 See Figure 8. 

Most of the blends of L calligraphus (treatments 7-10) and L avulsus (treatments 11-13) attracted 

L grandicollis, but at low levels. Vite et al. (1976) reported the lack of attraction of L grandicollis to 

ipsdienol alone, which indicates the importance of the blends to interspecific communication. However, 

while some research has shown the attraction of L grandicollis to bolts infested with L calligraphus 

(Vite et al. 1964, Birch et al. 1980, Svihra 1982) and L avulsus (Birch et al. 1980), other research has 

shown a lack of attraction (Vite et al. 1964, Birch et al. 1980, Svihra 1982). Without analysis of the 

volatiles from the bolts, of course, the blend of pheromones released in those studies cannot be 

determined. 

The blends of male and female D. frontalis (treatments 1-3) and D. terebrans (treatments 4-6) 

attracted L grandicollis. Significantly more (P > 0.05) L grandicollis were attracted to a combination of 

male and female D. frontalis blends (treatment 3) than to either blend alone (treatments 1 and 2). By 

comparison, significantly more (P > 0.05) L grandicollis were attracted to the blend of female 

D. terebrans (treatment 4) than to the blends of male D. terebrans (treatment 5) or male plus female 

D. terebrans (treatment 6). The attraction of L grandicollis to the pheromonal blends of both 

Dendroctonus species supports previous reports of the attraction of L grandicollis to frontalin plus 

trans-verbenol (Dixon and Payne 1980), as well as to D. frontalis-infested bolts (Vite et al. 1964, Birch 

and Svihra 1979, Birch et al. 1980, Dixon and Payne 1980, Svihra et al. 1980). 

365 
40 

> 3.0 Ips grand/col/Is 8 

.... 

~ • male 30 

~ F}J female 

~ 0 

u 2.0 

~ 20 += 

m 

co 

,..... 

w 

CJ) 

+I 

~ 1.0 10 c 

0 

Q) 

~ 

0.0 

1 2 3 4 56 7 8 910111213141516 17181920 

Treatment a 

Figure 12. Mean number of Ips grandicollis trapped in response to pheromonal 

compounds eluted at varying rates. 8 See Figure 8. 

As represented by turpentine alone (treatment 19), host odor did not provide an adequate 

stimulus to attract any of the scolytid species. It should be emphasized, however, that the release rate 

used was probably far less than that provided by a stressed tree in nature. In addition, the vertical 

silhouette alone (treatment 20), as provided by the unbaited trap, did not attract any of the five 

scolytid species. Thus the results verify that response by the beetles to the pheromone-baited traps was 

probably due to the pheromones and blends and not simply to host odor or to a visual stimulus alone. 

CONCLUSIONS AND INDICATIONS 

Detection of both Ips and Dendroctonus pheromonal compounds by the cohabiting species shows 

a sensory basis for their interspecific olfactory communication and interaction. The fact that 

differences in both threshold responses and relative numbers of receptors for the various behavioral 

chemicals do occur suggests differences in specific behavioral roles for each compound. 

The field tests showed variation in behavioral response among the species in interspecific 

olfactory communication. D. frontalis, the pioneering species of the group (Birch and Svihra 1979, 

Birch et al. 1980, Svihra et al. 1980), apparently does not utilize Ips pheromones in host selection. 

Cross-attraction of L calligraphus to male L avulsus, as of L avulsus to male L calligraphus, was 

366 
verified. However, given our results and the mixed results of the other reports cited, the attraction of 

1 calligraphus and 1 avulsus to 1 grandicollis or D. frontalis still remains in question. 1 grandicollis was 

the least specific in its responsiveness, displaying the greatest degree of cross-attraction among the 

cohabiting species. 

Although cross-attraction ranged from none for D. frontalis in response to the pheromonal 

blends of Ips to extensive for 1 grandicollis, it is probable that all five species benefit from the 

olfactory-based behavioral interactions. The interactions are probably most important when population 

levels are endemic, particularly for the less aggressive species, i.e. 1 grandicollis, when the joint efforts 

of the group members are essential for overtaking the defenses of the host trees. Certainly this would 

increase the probability of the successful colonization of a resistant host by each species. 

SUMMARY 

Interspecific olfactory response was investigated in the five primary scolytid species of the 

southern pine bark beetle guild, Dendroctonus frontalis Zimmermann, D. terebrans (Olivier), Ips 

calligraphus (Germar), 1 avulsus (Eichhoft), and 1 grandicollis (Eichhoft). Antennal olfactory response 

was measured with the electroantennogram and single-cell techniques and showed that each species 

possesses receptors most sensitive to their own pheromones, but also responsive to the pheromones of 

the other species. Behavioral responses were measured with field trap catch data and showed that each 

species was attracted mostly to the pheromonal blend produced by conspecifics. Interspecifically, 

D. frontalis showed no cross-attractancy to Ips pheromonal blends, but was attracted to the pheromonal 

blend of female D. terebrans. All three Ips species showed some level of cross-attraction as well as 

attraction to the Dendroctonus pheromonal blends. Specifically, 1 calligraphus was attracted to 

1 avulsus and slightly so to the male D. terebrans pheromonal blend. 1 avulsus was more crossattractive than 1 calligraphus and showed attraction to the pheromonal blends of female D. frontalis, 

male and female D. terebrans, male 1 calligraphus, and male 1 grandicollis. 1 grandicollis showed the 

greatest cross-attraction, particularly to the pheromonal blends of Dendroctonus. 

ACKNOWLEDGMENTS 

The authors are grateful to Bruce Buie, Department of Entomology, Texas A&M, for his 

assistance in conducting the research, to the U.S. Forest Service for help and permission to carry out 

the field tests in the National Forest, and to Dr. AC. Oehlschlager, Department of Chemistry, Simon 

Fraser University, and Semiochemicals International Ltd., Calgary, Alberta, Canada, for providing the 

enantiomers used in the study. The authors also gratefully acknowledge Janet Delorme, Phoebe 

Peterson, Virginia Brown, Susie Simerly, and Wilbur Long of the Department of Entomology, VPI, for 

their assistance in preparing the manuscript and personnel of the Statistical Consulting Center, 

Department of Statistics, VPI, for their efforts in data analysis. Finally, the authors gratefully 

acknowledge critical review of the manuscript by Drs. C.W. Berisford, University of Georgia, and 

R.F. Billings, Texas Forest Service. 

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368 
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PAYNE, T.L, ANDRYSZAK, N.A, WIESER, H., DIXON, E.A, ffiRAHIM, N., and COERS, J. 1988. 

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370 
USING PHEROMONES IN THE MANAGEMENT 

OF BARK BEETLE OUTBREAKS 

ALF BAKKE 

Norwegian Forest Research Institute 

Box 61, 1432 As-NLH, Norway 

INTRODUCTION 

Identification of aggregation pheromones and field experiments using synthetic components have 

given scientists a better understanding of the behavior of many bark beetles. They have also yielded 

more effective weapons with which to control outbreaks of aggressive pest species. Synthetic 

pheromone components are commercially available for control of many species (Borden 1985) and are 

used in forestry practice in several areas of the world (Vite and Francke 1985). The pheromone may 

be used as part of an integrated pest management program: for mass trapping, for monitoring of 

beetle populations, and for inhibition/disruption of beetle infestation. 

During the last 10 years we acquired valuable knowledge about the potential of pheromones for 

practical use. This paper summarizes some of the experience we have gained in our work with the 

spruce bark beetle, Ips typographus. 

THE PHEROMONE SYSTEM OF IPS TYPOGRAPHUS 

The spruce bark beetle, L typographus, is one of the most aggressive and serious pests of Norway 

spruce in Eurasia. There are two main reasons for their capacity to attack and kill healthy trees. 

First, they carry a pathogenic blue-stain fungi that invades the sapwood of the tree, induces water 

stress, and renders the tree susceptible to colonization by the beetles (Homtvedt et al. 1983). Second, 

they have developed an effective chemical signal system by which to coordinate the attack and to 

aggregate in masses on selected trees (Bakke et al. 1977, Schlyter et al. 1987). 

When the male beetle initiates the boring in the bark of trees, he produces a pheromone which 

attracts female beetles and other males. The two major components of the aggregation pheromone are 

(S) chaos-verbenol and 2-methyl-3-buten-2-ol. Ipsdienol, common in many Ips species, is also present, 

but seems to play only a minor role. Two components occur when the females have entered the 

gallery. These are ipsenol and verbenone, which inhibit response to the aggregation pheromone and 

act as an antiaggregation pheromone (Bakke 1981 ). 

MASS TRAPPING 

Mass trapping of bark beetles to suppress the population is a control measure that has been 

employed in Europe for more than 200 years. Until 1979 the trap used was a mature fresh tree which 

was felled in spring and left in the forest during the main flight period of the beetle. When the trunk 

had been colonized; by the beetles it was removed from the forest while they were still breeding in the 

BARANCHIKOV, Y.N., MA'ITSON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

371 
bark. After development of the synthetic pheromone and a trapping technology, the trap tree was 

replaced by the pheromone-baited trap (Bakke et al. 1983, Vite and Francke 1985). 

The Epidemic in Scandinavia in 1970-80 

Parts of southern Norway and Sweden suffered from an extensive beetle outbreak in the 1970s. 

In Norway, trees equivalent to 5 million cubic meters of timber were attacked and killed in an area of 

140,000 km2, which is equal to the area of East Germany. 

Extensive windthrow and severe summer drought combined to cause the outbreaks (Worrell 

1983, Bakke 1983). At the same time, many forest areas contained an abundance of overmature trees 

susceptible to beetle attack. 

Methods of the Control Program 

The pheromone of L typographus was identified in a research program conducted to search for 

methods to control the outbreak. Syntheses for commercial production of the pheromone were 

developed, and a method was devised by which to use the pheromones as bait in traps. A simple trap 

was designed to replace the trap trees (Bakke et al. 1983). 

In 1979, 600,000 drainpipe traps (Fig. 1) were produced and distributed in the outbreak area in 

Norway. Guidelines were developed for location of the traps. During 1979, 1980, and 1981 several 

billion beetles were trapped (Table 1 ). 

It must be emphasized that the use of traps alone was not recommended. Traps must be 

included in an integrated management program. In Norway several measures, both short-term and 

long-term, were undertaken during the outbreak period. Government funds were available for support 

of road construction in areas containing overmature stands and for logging in steep terrains. A forest 

practices law was amended to prohibit storage of unbarked logs in the forest during summer and to 

require cleanup after storm damage and logging. Besides the mass trapping, felling and removal of 

beetle-infested trees comprised the main short-term measure. Trapping was not recommended for 

saving old stands with extensive beetle infestation or stands severely weakened by drought. Only 

clear-felling was recommended for such stands (Nou 1979). 

The Trap Catches 

Average catches per trap varied widely between areas and years. In 1980, 10,000-12,000 beetles 

were the average catches per trap in districts with extensive beetle damage. Traps located at clearcuts 

from recent winter had the highest catches. During 1979-81 several billion beetles were trapped 

(Table 1). 

More than 99 percent of the insects caught in the traps were beetles of the genus L typographus, 

but a few percent of those caught in certain localities were L duplicatus which respond to ipsdienol. 

The clerids, Thanasimus formicarius and T. femora/is, are attracted by the pheromone (Bakke and 

Kvamme 1981) and were caught in some number even when the trap had been constructed to prevent 

them from entering through the holes. The average number of clerids per trap was 1.6 per thousand 

Ips in 1979 and 1.4 in 1980. A new trap model (1980 model) giving Thanasimus possibilities of escape 

retained only 0.5 clerids per thousand Ips. 

372 
No of beetles 

( 1000 ) 

20 

• 1 

18 

16 .-. 12.Scm .. 

.. 14 

135cm 

j 12 

10 

8 

6 

I. 

2 

! /!~ ----~-~/ !---~----! 

Years 1979 -80 -81 -82 -83 -81. -85 -86 -87 88 

Figure 1. Average catches of Ips typographus per trap on fresh c1earcuts in 

districts of southeast Norway during 1979 to 1988. The drainpipe trap is to 

the left. 

Socio-Economic Aspects 

A control campaign involving 80-100,000 private forest owners and people employed in forestry, 

covering the whole spruce area of South Norway and operating on government funds would have to 

confront problems in the areas of technology, economics, administration, and information dissemination. 

Technological Problems 

Trapping technology is, of course, an important part of a mass trapping program. The trap 

model must catch effectively, and pheromone release and composition must be optimal for the trap 

model. In addition, trap location and trap spacing must be evaluated, and traps must be inexpensive 

and easy to manage. Later studies (Bakke et al. 1983) have shown that we had good luck with the 

selection of our trap model, even though it had some weaknesses. Design of the dispenser and 

composition of the pheromone components had also been successfully estimated (Schlyter et al. 1987). 

Economics 

During the period from 1978 to 1982 the control program was supported by government funds 

totaling 90 million Norwegian Kroner, equivalent to 13 million 1988 U.S. dollars. Input from private 

forest owners came to at least that amount. The government paid 2!3 of the trap costs and about 1.5 

U.S. dollars per pheromone dispenser to the producers who had donated them to the project. A 

rough estimate of the total trapping cost incurred is 6 million U.S. dollars. 

373 
Table 1. Number of traps and estimated number of beetles caught in southern 

Norway in the years 1979-81 

Number of Estimated number 

Year traps of trapped beetles 

1979 600,000 2,900,000,000 

1980 590,000 4,500,000,000 

1981 530,000 2,100,000,000 

Administration 

The Civil Forest Administration was involved in the campaign in the counties and in every 

municipality. Committees were appointed on every administrative level. The local committee, headed 

by the district forest officer, coordinated the measures taken; decided on the number of traps each 

forest owner should deploy, and organized the search for infested trees, often by means of airplanes. 

The district officer also administered the government grant supporting the measures and provided the 

information to the local newspapers, television, and radio. 

Information 

Information about the control program was directed to the general public as well as the forest 

owners. Information was disseminated by means of leaflets, meetings and conferences, and newspaper 

articles. The drainpipe trap was used as the symbol of the program and had a great impact on public 

awareness. Seeing the thousands of beetles trapped in their forest, most forest owners in particular 

became aware of the hazard of retaining overmature trees. 

The general public had to be informed about the pipe traps they would encounter on their hikes 

in the forest. The function of the traps was explained in newspaper advertising campaigns and on 

radio and television. The information reached nearly everyone. The beetles even got their own pop 

song, "Bark-beetle Boogie," which placed on "top of the hits" in Norway for several weeks. 

The Decline of the Epidemic 

The epidemic began to decline after 1980, and in 1982 it was difficult to find trees killed by the 

beetle. The decline may have been caused by several factors, probably by a combination of factors 

(Bakke 1983). Cool and wet summer weather may have restored the resistance of the trees and limited 

the flight activity of the beetle. Though it is difficult to prove, we believe that the mass trapping 

campaign also had a significant impact on the beetle population. 

For a couple of reasons, the program is not easy to evaluate scientifically. We can estimate the 

number of trapped beetles, but we are unable to determine the size of the natural population. It is 

evident from several studies that the beetle disperses over large distances. Traps may be able to attract 

and catch most of the beetles within a certain area, but new beetles will quickly move in from 

surrounding areas to fill the vacated space. Actually to reduce the overall population, a larger area 

must be covered by a trapping program. Our experience further indicates that the most promising 

results are obtained with a low-density beetle population and in forests which are not too weak. 

374 
Today programs using pheromone-baited traps to maintain a low population of L typographus are 

established in several countries in Central Europe, among them the German Federal Republic, Poland, 

and Czechoslovakia (Zumr 1987). There, too, traps have replaced trap trees. 

MONITORING 

Aggressive bark beetles are a threat to the forest only when the population is above a certain 

threshold. The flying population must be high enough to overcome the resistance of a healthy tree. 

Knowledge of the population level is therefore of great importance, particularly when external 

conditions, such as long-lasting drought or stormfelling, favor population increase. Traps baited with 

pheromones may be useful in monitoring populations and in assessing the risk for damage caused by 

bark beetle. 

Research data for development of a monitoring system for L typographus have been gathered in 

Scandinavia in recent years. Different sites for deploying pheromone-baited traps have been studied 

and evaluated. The trapping period required to obtain a good estimate has also been studied (Bakke 

1985). 

A recently completed Scandinavian collaboration (Weslien et al. 1989) indicates that pheromonebaited traps as well as selected trees baited with pheromones have potential use in assessing the risk 

for damage caused by L typographus. 

The threat of damage to spruce forests in Central Europe as a result of air pollution, intensifies 

the need to monitor populations of other bark beetles as well (Vite 1984). Germany is using a system 

which combines monitoring with mass trapping to suppress beetle populations. In Norway, a 

monitoring system has continued since the great outbreak in the late 1970s. The mean catches per 

drainpipe traps during the years 1979-88 are given in Fig. 1. 

INHIBmON 

Pheromone components acting as inhibitors, lowering the attraction to the aggregation 

pheromone, are known in several bark beetle species. Best known is the MCH from L dendroctonus, 

which has been applied to windblown trees to prevent beetles from infesting the trunk (Furniss et al. 

1977). In addition, pine oil, a by-product derived from pulp mills, shows a semiochemical effect in 

bark beetle when sprayed on the bark surface of logs and trees (Nijholt 1980). 

In L typographus two pheromone components produced from the beetle have shown 

antiaggregative effect: ipsenol and verbenone. They are also known to inhibit attraction in other bark 

beetles (Bakke 1981). Combination of the two components produced the best inhibition effect when 

used together with the aggregation pheromone as bait in traps. 

Logs are stored for short or longer periods in the forest, often because in Scandinavia the snowmelting period in spring makes it difficult to use trucks in the forest. To prevent the logs from being 

infested by bark beetle and used for reproduction, the logs are often sprayed with insecticides. In 

Norway a field experiment was conducted during a 3-year period to determine whether any of the 

semiochemicals, when used in controlled release formulation on logs, are able to influence the 

colonization process of L typographus (Bakke 1987, Schlyter et al. 1989). 

All experiments showed that treatments with a combination of verbenone and ipsenol released 

from laminated structure dispensers significantly reduced the attack density of L typographus, whereas 

turpentine treatment had no effect on the rate of beetle infestation. 

375 
As applied in these experiments, with a rather high dosage of pheromones, antiaggregative 

semiochemicals may reduce beetle infestation in logs, but do not prevent logs from being attacked. As 

a consequence of reduction in population density, moreover, the survival rate of the brood may 

increase due to a more sufficient supply of food for the larvae. This would be very significant because 

overpopulation is a primary factor in mortality. On the other hand, the ipsenol acts as a kairomone 

(Bakke and Kvamme 1981) and may attract a larger number of the predator Thanasimus, which may 

eliminate a larger portion of the beetle and its brood. 

In my opinion, the pheromone will be an important part of the integrated management of 

several forest pests in the future. 

SUMMARY 

Bark beetle pheromone may be used in integrated pest management for mass trapping, 

monitoring of beetle population, and inhibition/disruption of beetle infestation. This paper reviews our 

experience in using both the aggregation pheromone and the antiaggregation pheromone for controlling 

L typographus in Norway. Drainpipe traps baited with synthetic aggregation pheromone components 

were used for mass trapping as part of an integrated control program during an epidemic. In 1980, 

4,500,000,000 beetles were trapped in 590,000 traps distributed in spruce forests in Norway. A 

monitoring program was developed using traps deployed on recent winter clearcuts. Application of 

antiaggregation pheromones to spruce logs stored in the forest during summer significantly reduced the 

attack density of spruce beetles, but the effect was not sufficiently great to make widespread 

implementation economically feasible. 

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WORRELL, R. 1983. Damage by the spruce bark beetle in South Norway 1970-80: A survey, and 

factors affecting its occurrence. Medd. Nor. Inst. Skogforsk. 38: 1-34. 

ZUMR, V. 1987. Reduction of mass outbreak in spruce bark beetle Ips typographus (L.) (Coleoptera: 

Scolytidae), by pheromone traps. Lesnictvi 33(1): 49-64. (In Czech with Russian and English 

summary.) 

377 
EFFECTS OF LARCH DEFENSES 

ON XYLOPHAGOUS INSECT GUILDS 

GALINA I. GIRS and VICTOR M. YANOVSKY 

V.N. Sukachev Institute of Forest and Wood 

Siberian Branch of the U.S.S.R. Academy of Sciences 

Krasnoyarsk 660036 U.S.S.R. 

INTRODUCTION 

One of the best studies of a xylophage consortium is the case of larch insects by Isaev and Girs 

(1975). In their book, a basic theory was presented about host responses to xylophagous insects injury. 

According to their concept of "sliding resistance," different trunk-infesting insect species have different 

reactions to the tree's defenses and invade the tree successively depending on the stage of its decline 

or dieback. With regard to the general tree status, groups of invaders were identified by the authors: 

1) primary species invading living trees whose resistance may increase back to the initial level; 

2) secondary species colonizing living trees with fatally disturbed metabolism, and 3) necrophagous 

species living only in dead trees. 

However, owing to its general nature, this classification cannot provide a detailed coverage of all 

the complexities arising when analyzing the ecological niche of xylophages. In particular, the potential 

increase in xylophage subcortical penetration rate was related mostly to the defense system of an 

individual tree without consideration of the environmental conditions (Sukachev 1967, Smagin et al. 

1980, Polikarpov et al. 1986). 

STAND FACfORS AFFECf XYLOPHAGES 

Certain groups of forest types have differential stress resistance and pronounced peculiarities in 

composition and structure of their xylophagous insect complexes (Y anovsky 1987). Thus, analyzing 

entomofauna within the framework of forest type classifications allows examination of both the 

peculiarities of the interaction between host tree and insects and interspecific relationships between 

insects: within ecologically homogenous insect groups (i.e. xylophages or phyllophages), between 

different insect groups (e.g. between xylophages and phyllophages) and also between phytophages and 

entomophages. Specific habitat conditions, plant defensive responses, both composition and structure 

peculiarities of a given biocenosis, as well as the insect "aggressiveness" determine outbreak probability 

and insect dispersal. All the above factors influence the rate of decline of individual trees and the 

total stand, and, thus, indicate the level probability for epidemics by the invading xylophage species 

(Yanovsky and Korotkov 1984). 

Deadwood load and distribution throughout the stand varies with forest type. So, food 

availability for sparse xylophagous insect populations and their dispersal patterns vary accordingly. At 

the same time, variations in the forest type response to the insect invasion and, consequently, tree 

dieback rate are responsible for the xylophage epidemic level. 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

378 
INTERACTIONS AMONG XYLOPHAGES 

Important also is the detailed analysis of xylophage interspecific relationships, with special regard 

to the primary infesting species located within a microstation (tree). Isaev and Girs (1975) divided the 

insect species into two groups based on their potential to overcome host defenses, disregarding the 

insect population density. Now we know that the aggressiveness of some insects varies with their 

abundance. Within the primary trunk infesting insect species two groups can be identified: 

1) xylophages capable of inhabiting the nonfatally declining trees, regardless of their population density, 

and 2) xylophages which can invade weakened trees only by means of severe, high density attacks. In 

the absence of severe stand damage, the first group dominates during the early stages of tree decline. 

These trees are inaccessible to the species of the second group so long as they remain at low 

population density. 

In case of a nonfatal tree declines, i.e. after surface fires, the species of the first group dominate 

xylophage complexes. They provide the conditions required for the attack of the second insect group, 

particularly if population density of the latter is low. This results in a sharp increase in the population 

density of insects of the second group, which the allows them to independently inhabit resistant trees. 

Burned Versus Defoliated Larch Forests 

These conclusions are consistent with the results of a study of xylophage outbreaks in the larch 

forests of middle Siberia, affected by fires (burned areas) and the siberian moth, Dendrolimus superans 

sibiricus Tschetv. In these stands the beetle, Tetropium gracillicome Rtt. and the larch buprestid, 

Phaenops guttulata Gebl. are representative of the primary insect species, capable of inhabiting 

non-fatally declining trees. On the other hand, the big larch bark beetle, Ips subelongatus Motsch., 

which is notorious for its violent population fluctuations, is incapable of invading trees with only slight 

metabolic disturbance unless it attacks en masse. 

Observations on the invading insect species groups at the early stage of stand decline show in 

defoliated stands, that the non-fatally declining larch trees are extensively attacked by the buprestids 

and Tetropium beetles that can overcome the host defense system and inhabit the trees with weakly 

disturbed metabolism (Table 1 ). Therefore, immediately after hatching, the nutrient status in the 

phloem is sufficient for larval feeding. The phloem physiological properties responsible for the 

oxidation processes do not differ noticeably from those of the control (Table 2). However, the free 

carbohydrate concentration in the phloem, that is vitally important for protein biosynthesis, is 

insufficient for the larval feeding due to the tree's low photosynthesis level. 

The bark beetles only inhabit the most weakened trees (Table 1 and 2). A few small 

populations of these insects were able to colonize trees with non-fatal metabolic disturbance, but the 

subsequent larval development was interrupted by pronounced resinosis (lsaev and Girs 1975). The 

bark beetle's ecological niche consists of slightly weakened larch trees with nonfatal metabolic 

disturbances. In this period a sharp increase in oxidation processes is observed, but enough 

carbohydrates are retained in the host phloem for the bark beetle larval feeding. 

The rate of stand decline determines the specific composition of the xyloj>hagous insect group. 

In the burned areas, where the stands are severely damaged by fires, the bark beetles dominate these 

groups immediately during the year of the fire (Table 1 ). It is noteworthy, that the trees infested with 

the bark beetles exhibit all the signs of total decline. The needles of these larches regenerating from 

dormant buds are pathological (too long and with water excess) and do not contribute much to tree 

recovery. But short-term physiological imbalance of trees does not allow bark beetle invasion. Under 

these conditions, hosts in early stages of decline are inhabited by buprestids. However, a lot of dead 

trees scattered throughout the burned area favor bark beetle buildups (lsaev and Girs 1975). For this 

379 
Table 1. Numbers of different xylophagous insects per sq dm of trunk in 

burned and defoliated larch stands over time 

Years after Mode of Attacked Insect population density1 

xylophage tree part of Phaenops Tetropium Ips subeoutbreaks decline trunk guttulata gracillicorne longatus 

B urn e d a r e a 

First Fatal Base 0.06 0.14 0.36 

Middle 0.02 0.86 

Top 1.04 

Second Fatal Base 0.09 1.09 

Middle 0.01 1.29 

Top 0.07 0.41 

Third Nonfatal Base 3.78 

M o t h d e f o 1 i a t e d a r e a 

First Nonfatal Base 1.97 2.04 

Middle 1.85 1.04 

Top 1.36 0.18 

Second Fatal Base 1.97 1.18 0.29 

Middle 2.39 0.15 0.25 

Top 1.77 0.05 0.05 

Third Fatal Base 0.42 0.45 2.00 

Middle 0.63 0.52 1.52 

Top 0.25 0.22 

Fourth Nonfatal Base 2.80 

1Number of larvae (Tetropium beetles and buprestids) or galleries (bark 

beetles) per 1 sq decimeter of trunk. 

reason, at the maximum xylophage population level (the second year after outbreak initiation) the 

primary insect group consists only of this one species (Table 1 ). 

Trunk Temperature Effects 

The bark beetle outbreaks are also likely to occur in the stands previously damaged by the 

phyllophagous insects, but in this case the bark beetles are competitively displaced by the buprestids 

and Tetropium beetles. Invasion and spread of buprestids in the moth-affected larch forests is retarded 

by the fact that the adults lay eggs on one and the same trunk part. Usually, the eggs are 

concentrated on the most weakened trunk part, arranged in strips on the southern side where phloem 

decline is facilitated by warming (Table 3). (See also Bombosch, this volume.) 

Increase in phloem surface temperature stimulates the general metabolic activity, which, in case 

of unstable metabolism, leads to the increase in oxidation and hydrolysis, protein decomposition, and 

380 
Table 2. Variations in tree phloem properties associated with invasion by various xylophagous species 

expressed as the actual values (AV) and as a percentage of the "control" host phloem (%) 

Phloem property 

State Moisture content Respiration rate Reducing capability Total sol. carbohydrate Starch 

of insect (~ fwt} (m& C02L&} (ml 0.01 N J!&} (~ dwt} (~ dwt} 

colonization AV % AV % AV % AV % AV % 

Phaenops guttulata and Tetropium gracillicorne 

Pre invasion 63.6 112 0.40 95 5.2 100 5.2 85 5.8 85 

Eggs 61.4 115 0.51 100 6.6 143 5.5 125 4.8 60 

Eclosion 63.4 106 0.58 232 4.4 100 6.6 129 4.9 45 

Larvae in 

phloem 31.5 58 0.25 61 1.1 24 2.8 42 4.2 24 

Ips subelongatus 

(j.l 

~ Oviposition 60.5 102 0.84 162 4.0 78 2.2 43 2.5 35 

Table 3. Variation in phloem properties on the north and south sides of infested trunks expressed as the 

actual values (AV) and as a percentage of the "control" host phloem (%) 

Side of trunk 

North (shaded side) 

South (sunny side) 

Temperature 

in day time 

( o C) 

21.9 

25.7 

Phloem properties 

Moisture content 

(% fwt) 

AV % 

53.8 

48.6 

80 

73 

Total sol. carbohydrate 

(% dwt) 

AV % 

7.5 

3.0 

59 

24 

Starch 

(% dwt} 

AV % 

3.2 

1.1 

32 

11 
decreases in tree defenses. The net result is that host phloem nutrient status is maintained high 

enough for the buprestid larval development. The phloem on the northern trunk part is wetter and 

richer in carbohydrates and starch. Here the insect penetration is time-delayed. Trees in similar 

conditions that fortuitously go uncolonized renew their needle next year and do not thereafter usually 

suffer from insect attacks. In trees with minimally disturbed metabolism, early subcortical penetration 

by the larch buprestids and Tetropium beetles is considerably interrupted by defensive biochemical and 

anatomical responses. The first instar larvae attempting to inhabit the phloem and adjacent wood layer 

are affected by a pronounced resinosis, followed by encapsulation of the larval galleries by the corked 

phloem cells. (See Herms and Mattson, this volume.) As the larvae grow in size their capsules grow 

longer and are oriented along the trunk (total length is 0.5 to 0.7 em). The capsule cavities are filled 

with resinous woody frass. This slow down the larval development rate, and increases mortality of the 

larvae in this period of time is up to 70 percent. The period of development of encapsulated 

buprestids and Tetropium larvae is considerably long. If the tree was inhabited late in summer, the 

larvae are expected to come out of the capsules in June next year. By this time the larvae are 2 to 

3 mm long and their most rapid development is observed in July (Table 4). Doubtless, the larval 

development is most rapid on the warmest (southern) side of the trunk. Here, the larval galleries are 

wide and meandering as can be seen from the gallery length and area measurements (Table 4). Quite 

in contrast, on the northern side of the host tree the larval galleries are narrower and run straight up 

and down. 

Due to this vertical direction of the larval galleries, the resin channels on the shaded side of the 

host plant are less damaged and, therefore, the larval mortality from resinosis is low. After being 

attacked by the Tetropium and buprestid beetles, the target trees exhibit a gradual decrease in 

resistance induced by the larval development. During the colonizing period and while larvae are 

encapsulated, the weakened trees do not differ greatly from the healthy ones in their physiological 

properties (Table 2). After this time the tree decline is obvious from the decrease in crown 

assimilation capability caused by the declining needle biomass followed by decreases in the phloem 

carbohydrate. The host plants show the first signs of decline by the time the larval emergence from 

capsules is over. This can be attributed to the general decrease in host viability manifested by reduced 

resin flow from the phloem resin channels. This, in tum, allows the larvae to extensively locate the 

intact zones of the phloem. On the other hand, the phloem destruction caused by the larval galleries 

leads to wound hyperoxidation which is evident from a sudden increase in respiratory rate, decrease in 

reduction capability, and gradual exhaustion of assimilant inflow which leads to decrease in 

carbohydrate concentration. These trees become attractive for the bark beetles. During the period of 

the young larval feeding, the host phloem suffers from a considerable water shortage. 

382 
Table 4. Development of larch buprestid larvae 

Side of Date of observation in Juli 

Development variables trunk 4 8 14 17 22 27 

Length of larvae (mm) South 5.2 0.7 9.3 12.0 12.7 18.0 

North 3.8 4.2 4.2 4.7 7.5 9.0 

Length of gallery (em) South 1.9 2.9 3.6 4.3 4.5 -* 

North 0.9 1.4 1.5 2.1 2.8 2.8 

Gallery area (cm2) South 0.51 1.12 1.99 2.21 3.21 -* 

North 0.17 0.18 0.35 0.67 0.79 0.80 

*Galleries join, making individual measurements impossible 

~.Table 5. ~ 

Variation in the larch phloem parameters in relation to bark beetle invasion expressed as the 

actual values (AV) and as a percentage of the "control" host phloem (%) 

Phloem property 

State of 

31 

21.3 

9.0 

-* 

4.6 

-* 

1.47 

bark beetle Moisture content Respiration rate Reducing capability Total sol. carbohydrate Starch 

colonization (~ fwt) (mg C02!g) (ml o.ol H J!s;l (~ dwt) (~ dwt) 

AV % AV % AV % AV % AV % 

Initial attack 62.5 104 0.40 91 3.8 80 2.2 43 4.9 76 

Oviposition 58.4 99 1.08 179 4.2 75 2.4 38 5.2 66 

Eggs and larvae 44.1 75 0.52 210 3.0 47 2.1 28 3.7 21 

Larvae 50.7 88 0.67 110 5.1 78 2.3 30 3.7 21 

Larvae and pupae 42.0 77 0.30 56 1.1 27 2.8 20 3.8 22 

Larvae to 

callow adults 35.0 62 0.32 74 0.6 14 0.3 3 0 0 
Bark Beetle Invasion of Trees 

The buprestids and the Tetropium beetles weaken the tree to the level suitable for the bark 

beetle survival. Distinguished by its high reproductive potential, that is being capable to produce much 

more generations per unit time in comparison with other insects, the bark beetle populations rapidly 

grow, competitively displace the buprestid and Tetropium beetles and become the dominant consumer. 

A significant difference between the bark beetles and other insects of interest lies in the way bark 

beetles injure the trees at high population density level. Symptoms of the declining host resistance 

become visible in the period of the bark beetle subcortical penetration and gallery construction. This 

period is characterized by the phloem hyperoxidation and total carbohydrate decline (Table 5). By the 

time the galleries are made the phloem tissues appear to be significantly damaged by the bark beetles. 

Crown isolation from the root system as well as the decrease of downward assimilant flow contribute 

to the host gradual dieback. During construction of larval galleries, the phloem moisture content, and 

the carbohydrate and starch concentration are reduced and the phloem turns brown owing to 

irreversible oxidation of many tissues (Table 5). The adult bark beetles are very capable of overcoming 

the host defense system, hence, they are largely responsible for the tree's defensive decline. A sharp 

decrease in the host defenses is observed during the mass larval hatching. At this stage of 

development the larval mortality is no more than 30 percent. Now the larval growth is no longer 

interrupted by the phloem defensive response. However, the phloem carbohydrate concentration 

remains comparatively high providing suitable conditions for the larval feeding and development. 

It can be concluded that examination of xylophage group composition at the time of an 

outbreak allows one to predict the extent of decline both the individual tree and total stand. Sparse 

populations of the Tetropium and buprestid beetles located on resistant trees indicate that reduction of 

tree defenses below a critical level may allow bark beetle infestation to follow. On the other hand, the 

subcortical penetration of the low density bark beetle populations predict an ominous future for the 

stand. 

LITERATURE CITED 

ISAEV, AS. and GIRS, G.I. 1975. The host-xylophage interaction. Vzaimodeistvie dereva i nasekomykh 

- khsilofagov. Novosisbirsk: Nauka. 344 p. (In Russian.) 

POLIKARPOV, N.P., CHEBAKOV A, N.M., and NASIMOV A, D.I. 1986. Climate and mountain forests 

in southern Siberia. Novosibirsk: Nauka. 226 p. (In Russian.) 

SMAGIN, V.N., IUINSKAYA, S.A, NAZIMOVA, D.I., NOVOSELTZEVA, I.F., and 

CHEREDNIKOV A, Ju.S. 1980. Mountain forest types in southern Siberia. Tipy gomykh lesov 

yugnoji Sibiri. Novosibirsk: Nauka. 336 p. (In Russian.) 

SUKACHEV, V.N. 1967. Biogeocenology and its actual problems. Zhumal obshei biologii 28, 

5: 501-509. (In Russian.) 

Y ANOVSKY, V.M. 1987. Variations in the requirements between plants and xylophagous insects as 

forest ecosystem stability indicator. p. 5-16. In Ekologicheskaya otzenka mestoobitanii lesnykh 

zhyvotnykh. Novosibirsk: Nauka. (In Russian.) 

Y ANOVSKY, V.M. and KOROTKOV, I.A 1984. Biozenotic patterns of forest pest outbreaks in 

Mongolia. Lesovedenie 4: 35-41. (In Russian). 

384 
EFFECfS OF FIR SAWYER BEETLE 

ON SPATIAL STRUCIURE OF SIBERIAN FIR STANDS 

VLADIMIR L. GA VRIKOV and VALENTINA P. VETROVA 

V.N. Sukachev Institute of Forest and Wood 

Siberian Branch of the U.S.S.R. Academy of Sciences 

Krasnoyarsk 660036 U.S.S.R. 

INTRODUCTION 

Insects not only use plants for food and habitat; they also change plant populations by 

influencing their structure and dynamics. This influence is evidenced in the alteration of the spatial 

structure of a stand. 

The fir sawyer, Monochamus umssovi Fisch. (Coleoptera: Cerambycidae), is the most abundant 

xylophagous insect injuring siberian fir, Abies sibirica Ledeb. It dominates both in outbreak and nonoutbreak areas. The beetles influence the structure and dynamics of fir stands by damaging tree crowns 

during adult feeding. At high population density this damage eventually determines the spatial 

structure of the fir stands. 

METHODS 

We sampled plots on a western slope in the taiga zone of the Western Sayan mountains, South 

Siberia, U.S.S.R. In this habitat, siberian fir is a climax species that successfully reproduces under its 

own canopy. 

To estimate the spatial pattern of fir stands, we used two sample plots (1 and 1.5 ha), with 

1,000 and 2,000 fir trees, respectively. The first plot was an all-aged fir stand with an age distribution 

described by a rather smooth, inverse J-shaped curve. The second plot was an uneven-aged fir stand 

with a bimodal curve of age distribution. The first plot was inhabited by sparse populations of 

M. urussovi and the second by a very dense population. 

We obtained coordinates of all fir trunks within the plots as well as their parameters and used 

the radial distribution function to interpret the data statistically. We used a version of the technique 

and computer programs modified by Dr. O.P. Sekretenko (Buzykin et al. 1985). Radial function of 

distribution G(r) characterizes probability in order to find a point at a distance from r to r + dr away 

from a randomly chosen point on a plot map. A simple modification of G(r) allows us to study 

mutual arrangement of trees classified into two groups. This technique is known as partial radial 

distribution function. This function characterizes the probability of detecting an object of one class at 

a distance from r to r + dr away from a randomly chosen object of the other class. 

We have obtained the partial radial function of distribution of 40- to 60-year-old fir trees in 

relation to dead, standing trees damaged by the fir sawyer and vigorous trees of the crown layer. The 

radial distribution function of the young trees over the plots has also been calculated. 

BARANCHIKOV, Y.N., MA'ITSON, WJ., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

385 
RESULTS AND DISCUSSION 

To date no direct observations have been made of the behavior of adult fir sawyers during 

colonization of a forest stand. We have assumed that adults normally fly a short distance away from the 

place of emergence. 

In the stands we examined, the fir sawyer damages mature, but not young trees. This critical feature 

of host selection allows a self-replacement process in the fir population. The pattern of establishment and 

growth of seedlings and the mortality of mature trees determine the structure of a fir stand. In the 

all-aged fir population a low asynchronous mortality is observed. Under these conditions, the 

micropopulations of the sawyer colonizing the dying trees appear to be spatially separated. Hence tree 

crowns neighboring the infested ones are damaged rather lightly and the trees are not weakened 

sufficiently to allow for egg laying. Since the fir sawyer attacks only the naturally dying trees or 

occasionally those weakened by other factors, sparse populations of fir sawyer are maintained. 

In the second fir stand, old trees predominate, which results in increased mortality of mature fir 

trees and a higher density of fir sawyer population. There is some evidence of beetle concentration on 

weakened trees and of localized insect distribution for adult feeding and oviposition (Vetrova 1986, 1987). 

Intensive crown damage (5 to 9 grazing wounds per 1m of first-order branches) resulted in irreversible 

tree weakening. The damaged trees were then attacked by ovipositing females. High colonization density 

(up to 7 eggs per 1 sq dm) is observed. We believe that beetle activity explains the patchy distribution of 

infested fir trees that we observed (Fig. 1). 

A 

f,5 

..._'o 

<( .. •.o 

Ec.n 

,._.... 

X 

0 B 

l: 2,0 

LU 

0 

>< 

z 

1,0 

~ 

0 

fOO 200 300 400 500 

SIZE OF RECORD PLOT,m2 

Figure 1. Spatial distribution of infested trees on the sample plots. 

I 6 = q [ Er:J/C~ ~)l)] , where q - number of record plots, n 1 = number of trees 

on a record plot, N - number of all trees on a sample plot, A and B - habitats 

of the beetle populations (A= dense population, B =sparse one). 

386 
Gtr) 

2 

1 

A 

0~----~------~------~------_. 2 

' 10 '' 20 r,m 

G(r) 

:ri--I=L-~~~~-~=- o~----~~----~--------------~ tO fJ 20 

2 

r,m 

Figure 2. Spatial distribution of young fir trees in relation to standing 

dead trees (a) and undamaged old ones (b). G (r) - radial function of 

distribution (see text), r- radius of a record plot, A and B - quantities 

shown in Fig. 1. 

GCr) 

' 

2 

1 

0 .__ __ ___._ ____ ___._ ____ ~-----'---- 2 

G(r) 10 1; eo r,m 

~ 

2 

1 

0 

' 10 

B 

,, 20 

2 

r,m 

Figure 3. Histograms of radial function of distribution of young fir trees. 

G(r) - radial function of distribution (see text); other symbol codes as in 

Figs. 1 and 2. 

387 
A relation between the distribution of young (40- to 60-year-old) trees and standing dead trees 

exists such that the partial radial function. of distribution shows a positive correlation in relative mutual 

arrangement of these two groups (Fig. 2). If so, we should expect different parameters of spatial 

distribution of young fir trees in the stands we examined. In fact, we observed more clustered 

distribution of young trees in the fir stand of the second type, as can be shown in Fig. 3. 

In the habitat of the sparse sawyer population, the tree mortality pattern of mature trees results 

in rather small patches of young trees (not more than 50 sq m). Large patches of dying trees occur 

when the fir sawyer population are high and consequently cause larger patches of young tree (up to 

200 sq m). 

From the reports of other authors on the ecology of M. urussovi, it is clear that the case of 

outbreak populations of the beetle sharply differs from the above (lsaev et al. 1985, 1988). Usually, 

outbreak populations cause a constantly high mortality rate of mature trees. Spatial dynamics of fir 

stand damage look like the spreading of a single wave, comparable sometimes to that of fire. 

CONCLUSION 

M urussovi F. is an important factor in the spatial and age dynamics of A. sibirica stands. 

Sparse beetle populations do not disturb the asynchronous, all-aged pattern of fir stand structure and 

do not prevent the fir population from achieving stability. On the other hand, high-density populations 

of the fir sawyer, accelerate the mortality rate of mature trees, giving rise to relatively widespread, local 

synchronization of fir tree development and decrease the stability of the whole system. 

LITERATURE CITED 

BUZ¥lGN, AI., GA VRIKOV, V.L., and SEKRETENKO, O.P. 1985. Analysis of structure of the tree 

populations, p.1-94. In Analiz struktury drevesnykh cenozov. Novosibirsk: Nauka. (In Russian.) 

ISAEV, AS., KISELEV, V.V., OVTCHINNIKOVA, T.M., and KHLEBOPROS R.G. 1985. Model of 

distribution of fir sawyer beetle outbreaks, p. 135-144. In Matematicheskaya biofysika. 

Krasnoyarsk: KGU. (In Russian.) 

ISAEV, AS., ROZHKOV, AS., and KISELEV, V.V. 1988. Fir sawyer beetle Monochamus urussovi 

Fisch. Bolschoi khvoinyi usach Monochamus urussovi Fisch. Novosibirsk: Nauka. 264 p. 

(In Russian.) 

VETROV A, V.P. 1986. Effect of low and high-density populations of the fir sawyer (Monochamus 

urussovi Fisch.) on fir stands. Lesovedenie 1: 43-50. (In Russian.) 

VETROV A, V.P. 1987. The role of stand state in consortive relations of fir sawyer beetle and siberian 

fir, p. 106-115. In Ekologicheskaya ocenka mestoobitaniya lesnykh zyvotnykh. Novosibirsk: Nauka. 

(In Russian.) 

388 
FIR SAWYER BEETLE-SIBERIAN FIR 

INTERACfiON MODELING: 

RESISTANCE OF FIR STANDS TO INSECf OUTBREAKS 

TAMARA M. OVTCHINNIKOVA and VICfOR V. KISELEV 

V.N. Sukachev Institute of Forest and Wood 

Siberian Branch of the U.S.S.R. Academy of Sciences 

Krasnoyarsk 660036 U.S.S.R. 

INTRODUCTION 

Entomological monitoring is part of a total ecological monitoring system. Its purpose is the 

identification, prognosis, and estimation of forest ecosystem impacts induced by insects. The 

entomological monitoring of a forest is based on a clear understanding of the role played by insects in 

forest ecosystems. The patterns of insect population dynamics in space and time have to be discovered. 

Mathematical models can be used to make a prognosis and determine the components and parameters 

of a given system. 

SAWYER BEETLE BIOLOGY 

After monitoring fir forests in the northeastern part of the U.S.S.R., we present here a 

mathematical model describing an outbreak of Monochamus urussovi Fisch. (Cerambycidae: Coleoptera). 

It is known that food availability is the major factor determining population density of this sawyer 

beetle and other xylophages. Sawyer beetles generally colonize only weak and dying trees, where the 

larvae of this species develop. The adult insects feed in the crowns on the thin bark of branches, and 

in so doing causes branches to dry out. When the feeding damage is considerable, the tree weakens 

and becomes suitable for oviposition and larval feeding. In a resistant forest ecosystem, the variations 

in sawyer beetle populations are determined by the variations in availability of weakened trees for 

infestation. Population density is regulated by the negative feedback principle. The population was in 

a stable state at the time of our study. During a sawyer beetle outbreak the high beetle numbers 

decrease the resistance of normally vigorous trees, and this positive feedback results in expansion of the 

outbreak area. If the process of forest destruction is stabilizing, the sawyer beetle population achieves 

a hyperstable state. 

MODELING BEETLE-STAND INTERACTIONS 

Our simulation model of the "stand-beetle" system takes into account patterns of interaction 

between sawyer beetles and separate fir trees at different stages of damage. The system variables are: 

number of imagos (N), food supply (F) for imago, and food supply for larvae (D). A system of three 

discrete equations describes the interaction of insects with separate trees. The beetles colonize the 

most attractive trees surrounding the one from which they have emerged. The attractiveness of a tree 

is a function of the extent of damage to the tree by the beetles and is determined from the 

BARANCHIKOV, Y.N., MATI'SON, W.J., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

389 
experimental data. The parameters of the system are 1) the dimensions and condition of the tree, 2) the 

time when the tree is suitable as a food resource, 3) survival during ontogenesis, 4) fecundity, 5) sex ratio, 

6) time of pre-imago development, and 7) migration characteristics. 

The model is solved through a set of computer programs. Simulation experiments allow us to study 

the dynamics of a system in space and time. The system may be in one of two states: stable or 

hyperstable. Transition from one state to another is related to the transition of the parameter values from 

below to over threshold values. We have shown that the stable state of a system is achieved as a result of 

natural random dying of trees. The hyperstable state takes on the form of running waves of sawyer beetle 

densities and food resources. Threshold values exist for the initial imago density, annual rate of food 

consumption per one beetle (Ro ), initial food resources, and some others. Crossing of a threshold 

transforms a system from a stable state into a hyperstable one. 

We have found that a metastable state can occur only in stands with a certain defined structure. A 

tree is suitable for colonizing when the ratio of damage by beetles to the crown during adult feeding is 

greater than a critical ratio. This critical ratio depends on the values of N, F, and Ro. The greater the 

ratio between imago density and food supply in the crown, the greater the probability of positive feedback 

in the system, and, consequently, of an outbreak. 

In the hyperstable state, the number of emerged imago at some selected part of the forest is 

determined by the total identifiable food supply for larvae. This number was obtained from the 

experimental data on the relationship between the number of emerging imagos and tree diameter (d) and 

n 

is equal to E k1(d), where k1(d) is the number of imago emerging from the tree with diameter, d, and n 

i=l 

is the number of trees in the given part of the forest. The food supply for imago in the same part of the 

n 

forest is equal to E F1(d,P), where F(d,P) is the food supply in the crown of a tree with diameter, d, and 

i=l 

Pis the stand density. We have introduced the parameter, 71 = E k1 IE F1, to characterize fir stand 

resistance to sawyer beetle damage. Classifications of stable and unstable stands are made using this 

parameter. Increase in the mean diameter and density of a stand indicates an increase in the probability of 

an outbreak. 

390 
CONIFER DEFENSES AND XYLOPHAGOUS INSECTS 

ALEXANDR S. ROZHKOV and GALINA I. MASSEL 

Siberian Institute of Plant Physiology and Biochemistry 

Siberian Branch of the U.S.S.R. Academy of Sciences 

Irkutsk 664033 U.S.S.R. 

INTRODUCTION 

The resistance of woody plants to phytophage damage consists of a universal system of 

mechanisms: 1) repellent chemicals, 2) defensive reactions both mechanical and chemical, 3) retention 

of viability under disturbed metabolism and low biomass accumulation, and 4) recuperative capacity. 

Siberian coniferous tree species, with the exception of Larix, are less resistant to phytophage 

damage than deciduous ones. Evergreen conifers evolved toward constitutive antibiosis by improving 

their chemical mechanisms of defense, i.e. terpenoid repellents and toxins. In deciduous species, there 

was evolution of defenses in the direction of an increase in tolerance and recovery (especially after 

damage or loss of assimilation organs). The universality of the protective mechanisms of woody plants 

is manifested in the nonspecificity and the relative uniformity of their responses to the different agents 

of injury (biotic, chemical, or mechanical). 

We have tried to correlate the main stages of tree decline with tree metabolic and resistance 

changes (Fig. 1 ). The number of eliciting damage sources could be extended to include drought or 

disturbances in soil conditions, but the five categories of tree conditions shown in Fig. 1 were 

determined to be adequately representative of the processes involved. 

STAGES OF TREE DECLINE 

Each successive stage of decline in tree resistance is characterized by certain biochemical 

transformations. During the first stages of injury, under excited but not reduced metabolism, the levels 

of resins, a number of mono- and sesquiterpene hydrocarbons, quinic and shikimic acids, polyphenols, 

tannins, some amino acids (e.g. proline), increase in the inner bark. For a while, the increase in these 

substances stimulates the protective system to a level exceeding its initial level. Even the most 

aggressive xylophages fail to colonize such trees. 

The prolonged defensive responses result in a decrease in biomass synthesis and hence in 

insufficient repair of the photosynthesizing, conducting, and storage systems. In such a weakened tree 

with reduced metabolism, the synthesis of protective toxins begins to decrease. In the majority of 

cases, a decrease of delta-3-carene and an increase of a-pinene takes place. The diminution of the 

resin "barrier• in conifers colonized by xylophages can be accounted for mainly by the overall content 

of resinous substances in the inner bark and the involvement of their neutral fraction. The 

concentrations of specific toxic components of the essential oils are also significant. 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

391 
healthy 

Cfl 

IZl weakened 

IZl :a 

~ til 

E-4 

H 

Pri 

0 14 

sick 0 ~ 

0 j:q 

H 

E-4 ell 

H E-4 

A 

~ seriously ~ 

0 sick 

lli Cll 0 

IZl 

~ 

irreversible 

damage 

normal 

level 

excited 

reduced 

low 

discoordinated 

Inherent resistance 

Increase ot 

defence Reparation 

Insufficient Limit of ac- tive defence accumulation 

of biomass 

Tolerance High catabolism 

Extinction Death 

Figure 1. Correlation of tree decline stages with changes in tree metabolism 

and resistance. 

The severely weakened tree is accessible to attack both by aggressive xylophage species and by 

species otherwise susceptible to its defenses (mainly conifer oligophages). In many cases, this stage of 

tree damage culminates in irreversible disturbance of the tree's metabolic processes without any 

additional damage by insects to the trunk tissue. This state of irreversible damage is characterized by a 

very low level of resins and resin activity. Larch, pine, and fir trees become nonviable when their resin 

level has fallen to 1 to 2 percent, 3 to 4 percent, and 4 to 5 percent, respectively. 

392 
ATIRACfiON OF SOME SCOL YTIDS 

AND ASSOCIATED BEETLES 

TO THE HOST VOLATILES a-PINENE AND ETHANOL 

LEIF MARTIN SCHROEDER 

Swedish University of Agricultural Sciences 

Division of Forest Entomology, S-750 07 Uppsala, Sweden 

INTRODUCTION 

Several scolytid species are known to use host volatiles such as monoterpenes and the 

degradation product, ethanol, when searching for suitable host material. The release rates of terpenes 

and ethanol and the proportions in which they are released can be expected to differ depending on the 

breeding substrate preferences of the various scolytid species. 

The· aim of this study was to compare the attraction of various scolytid species and associated 

beetles to combinations of a-pinene and ethanol in proportions of approximately 1:1 and 1:10 when 

released at three different rates. a-Pinene was chosen because it is one of the major monoterpenes in 

both Scots pine, Pinus sylvestris L, and Norway spruce, Picea abies (L.) Karst., the two dominant 

conifers in Scandinavia. Ethanol was chosen because it is one of the major degradation volatiles which 

are produced as a result of deterioration processes in dead or dying trees. Both substances have 

previously been demonstrated to attract several wood- and bark-living beetle species. 

EXPERIMENTAL METHODS 

The attraction of beetles to the different compounds or combinations of compounds was 

estimated using baited flight-barrier traps (40 x 40 em transparent plastic sheets). The chemicals used 

were (-)-a-pinene (Fluka 97 percent) and 95 percent ethanol (5 percent water). The substances were 

released at different rates from polyethylene vials with different-sized openings. After combinations of 

a-pinene and ethanol had been tested, the two substances were released from separate vials. To 

minimize release of oxidized substances during the experiment, new vials containing fresh compounds 

were exchanged for old ones on each day of the experiment. A randomized block experimental design 

was used in the arrangement of the experiment. There were 10 blocks, and each block consisted of 

14 treatments (traps). The following types of treatments were used: unbaited control, three release 

rates of a-pinene (0.1, 1, 10 mg/hr), four release rates of ethanol (0.1, 1, 10, 130 mg/hr), and the 

1:1 and 1:10 combinations of a-pinene and ethanol at the three a-pinene release rates. 

RESULTS 

With the exception of Anisandrus dispar (F.), all scolytid species involved in the study breed in 

conifers. A. dispar, which breeds in dead or dying trees of several hardwood species, was the only 

species that was repelled by the conifer monoterpene, a-pinene. A. dispar was strongly attracted to 

e.thanol alone. 

BARANCHIKOV, Y.N., MATfSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

393 
In contrast to the other scolytids in this study, Tomicus piniperda (L.) generally breeds in 

relatively fresh material, e.g. newly windbroken or windthrown trees and winter- or spring-cut logs. 

Since such material has only just begun to deteriorate, the release of ethanol should be rather low, 

while high amounts of terpenes may be released from resin exuding from damaged parts. Accordingly, 

T. piniperda was the species most strongly attracted by a-pinene alone. Ethanol also attracted this 

species, but to a much lesser degree than a-pinene. T. piniperda was synergistically attracted to 

combinations of a-pinene and ethanol at the two lowest release rates of a-pinene. At the highest 

release rate of a-pinene, the combinations caught lower numbers of T. piniperda than did a-pinene. 

Evidently, attraction cannot be increased funher by adding ethanol to a-pinene at this high release 

rate. 

The scolytids Hylurgops palliatus (Gyll.) and Trypodendron lineatum (Oliv.) generally reproduce in 

dead or dying trees. They prefer logs cut during autumn of the previous year over newly cut logs. 

This type of stored breeding material may release relatively high amounts of ethanol produced in 

deteriorating tree tissue, while monoterpenes are probably released in lower amounts compared with 

the amounts released from newly felled or broken trees. As expected, neither H. palliatus nor 

T. lineatum was attracted as strongly to a-pinene alone as was T. piniperda. The ambrosia beetle 

T. lineatum was not attracted at all by a-pinene, but was strongly attracted by ethanol which exened a 

weaker attraction on H. palliatus. Both species were synergistically attracted to combinations of 

a-pinene and ethanol. The synergism was strongest when the release rate of ethanol was 10 times 

higher than that of a-pinene. 

Adults of the clerid Thanasimus formicarius (L.) prey on adults of several species of bark 

beetles, and their larvae feed on bark beetle progeny. The wide range of prey species, which in their 

tum are attracted to different kinds of breeding material, may explain the fact that T. formicarius was 

as strongly attracted to a-pinene alone as to combinations of a-pinene and ethanol. 

The nitidulid beetles Glischrochilus quadripunctatus (L.) and Epuraea spp. were significantly 

attracted to a-pinene and ethanol alone, but much higher numbers of beetles of these species were 

attracted to the combinations, especially when the ethanol was released at a higher rate than the 

a-pinene. G. quadripunctatus and Epuraea spp. are species associated with bark- and wood-living 

beetles. Adults and the progeny of these species inhabit scolytid galleries. In this kind of substrate, 

deterioration processes should result in a gradual increase in the production of ethanol, released 

together· with host terpenes. This may explain the strong synergistic effect of combinations of a-pinene 

and ethanol on attraction in these species. 

CONCLUSIONS 

The present study demonstrates great differences between beetle species in their response to 

a-pinene, ethanol, and combinations of the two. These probably reflect the dissimilarities in the 

release of volatiles among the various types of breeding material to which the different species are 

adapted. Both the absolute release rates and the ratios at which the two substances were released 

influenced the response of the beetles to the combinations. 

A more detailed presentation of the experiments and the results is given in Schroeder (1988) 

and Schroeder and LindelOw (1989). 

394 
LITERATURE CITED 

SCHROEDER, LM. 1988. Attraction of the bark beetle Tomicus piniperda and some other bark- and 

wood-living beetles to the host volatiles a-pinene and ethanol. Entomol. Exp. Appl. 

46: 203-210. 

SCHROEDER, L.M. and LINDELOW, A. 1989. Attraction of scolytids and associated beetles by 

different absolute amounts and proportions of a-pinene and ethanol. J. Chern. Ecol. 

15: 807-817. 

395 
INFLUENCE OF PREDATORS AND PARISITOIDS 

ON BARK BEETLE PRODUCTIVITY 

JAN WESLIEN 

Division of Forest Entomology 

Swedish University of Agricultural Sciences 

P.O. Box 7044, S-75007 Uppsala, Sweden 

In an earlier field experiment, natural enemies of the bark beetle, Ips typographus (L) were 

estimated to have reduced bark beetle productivity by more than 80 percent. To test this hypothesis, 

spruce logs (Picea abies) were placed in the forest in the spring, prior to commencement of flight by 

1 typographus. The logs were screened at different times following onset of bark beetle attack. The 

screens prevented further colonization by bark beetles and associated insects. The insects were 

subsequently collected as they emerged from the logs the following autumn or the following spring. 

The treatments used were as follows: 

C = Control, screening prior to attack, bark beetles released on logs under the screen 

E.S. = Early screening, 1 week after first bark beetle attack 

I.S. = Intermediate screening, 4 weeks after first attack 

LS. = Late screening, 8 weeks after first attack. 

The earlier the screening was done, the more bark beetles emerged from the logs. The mean 

number of juvenile imagos of 1 typographus emerging was 2800/m2 from the control logs, 2300/m2 

from the E.S. logs, 1200/m2 from the I.S. logs, and only 460/m2 from the LS. logs. Mean attack 

densities were similar for all treatments: 230-240 nuptial chambers/m2. Therefore, the differences in 

bark beetle emergence between the treatments cannot be explained by varying degrees of intraspecific 

competition. 

Virtually no predators and parasitoids emerged from the control logs and very few from the 

E.S. logs. Overall, the later the screening was done, the more predators and parasitoids emerged. 

The most important predator was Medetera spp. (Diptera: Dolichopodidae ), which emerged at a 

mean rate of about 170 imagos/m2 from both I.S. and LS. logs. The most important parasitoids were 

Roptrocerus spp. and Rhopalicus spp. (Hymenoptera: Pteromalidae ), which together emerged at a mean 

rate of about 50 imagos/m2 from the I.S. logs and about 340 imagos/m2 from the LS. logs. 

Other insects which emerged were Thanasimus spp. (Coleoptera: Cleridae), eight larvae/m2 

emerging from I.S. logs and 18 larvae/m2 from L.S. logs; small staphilinid larvae--mostly Phloeonomus 

spp. and Placusa spp.--(Coleoptera: Staphilinidae)--60 larvae/m2 emerging from I.S. lo~ and 

150 larvae/m2 from L.S. logs; and Lonchaea spp. (Diptera: Lonchaeidae), 55 imagos/m2 emerging from 

L.S. logs. 

In contrast to other insects emerging, Epuraea spp. (Coleoptera: Nitidulidae) were abundant in 

E.S. logs, about 380 larvae/m 2, but scarce in logs screened later. This may indicate that late-arriving 

insects preyed also on Epuraea larvae. 

BARANCHIKOV, Y.N., MA'ITSON, WJ., HAIN, F.P., and PAYNE, T.L, eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

396 
SEASONAL AND SPATIAL CHANGES 

IN THE STRUCfURE OF THE SUBCORTICAL 

INSECf COMMUNITY IN PINE FORESTS 

KEN YOSHIKAWA and MAKOTO KASAHARA 

Laboratory of Silviculture, Faculty of Agriculture 

Kochi University 

Monobe B200, Nankoku City, Kochi, Japan 783 

INTRODUCTION 

More than 30 species of beetles have been identified/documented as pine borers in Japan, the 

majority of them belonging to the Curculionidae, Cerambycidae, and Scolytidae. The density of their 

populations is controlled primarily by food supply. Although most of them are secondary pests which 

cannot attack healthy trees, an epidemic of pine wilt disease caused by the pine wood nematode, 

Bursaphelenchus xylophilus, has guaranteed them a continuously sufficient food supply. This paper 

discusses the results of an experiment to study seasonal and spatial changes in the structure of the 

subcortical insect community in pine forests. 

EXPERIMENTAL METHODS 

The study was conducted in pine forests along the ridge of a group of hills extending 8 km 

inland from the seashore (Fig. 1). Traps made of black vinyl chloride and baited with a-pinene and 

ethyl alcohol were used to attract flying adult beetles. Eight traps were set up in 1985 and seven traps 

were added the following year. The traps were placed 1.5 m above ground to facilitate evaporation of 

the attractants, a-pinene and ethyl alcohol. the dominant species of pine in the area under study 

shifts from Pinus thunbergii in the coastal region to P. densijlora in the inland area. 

RESULTS AND DISCUSSION 

Fauna 

More than 1,300 specimens of Cerambycid beetles were captured during three seasons. They 

were classified into 36 species and 28 genera. The dominant three species, Monochamus alternatus, 

Spondylis buprestoides, and Arhopalus coreanus, accounted for about 65 percent of the total catch. 

Weevils were classified into 59 species and 42 genera belonging to four families, Curculionidae, 

Rhynchophoridae, Anthribidae, and Apionidae. Fifteen species, representing 95 percent of the total 

catch, can attack pine trees (Shikoku Branch Gov. For. Exp. Stn. 1962). About 85 percent of these 

specimens belonged to the genus Shirahoshizo, which includes Sh. insidiosus, Sh. pini, and Sh. rufescens. 

The ratio among the number of these three species was 53:28:19. 

Scolytidae and Platypodidae were classified into 52 species and 14 genera. About one half of 

them (14 out of 29 identified species) belonged to the group of ambrosia beetles. Eleven species can 

BARANCHIKOV, Y.N., MATTSON, W.J., HAIN, F.P., and PAYNE, T.L., eds. 1991. Forest Insect 

Guilds: Patterns of Interaction with Host Trees. U.S. Dep. Agric. For. Serv. Gen. Tech. Rep. NE-153. 

397 
Study area 

and traps 

Figure 1. Trap and trapping sites along an 8 km ridge. 

feed on pine trees (Yasunaga 1964, Nobuchi 1966, Hayashi et al. 1984). Taenioglyptes fulvus, Tomicus 

piniperda, and Xylosandrus crassiusculus were the main pests and they accounted for 89 percent of the 

total catch. 

Although a-pinene is the principal attractant forM. alternatus, almost all other species were 

attracted to a-pinene. Thus a-pinene appears to be an effective tool for investigating the subcortical 

insect community. 

Changes in Abundance 

Temporal and spatial niche segregations were observed among the dominant species of the three 

groups--the cerambycids, the weevils, and the scolytids. 

Seasonal Changes 

In the cerambycid community, M. alternatus and Sp. buprestoides were the first to commence 

flight (Fig. 2A). As the flight period of Sp. buprestoides was not long, the ratio of this species 

decreased in August, as that of A. coreanus increased. In September, A. coreanus amounted to about 

60 percent of the total catch. 

398 
A B c 

4 

H. '""····· 3 

2 

., 

~ 

., 

., 0 

•of 

40 Ta. lwh•• 

30 "· ......... 30 

:;~ 20 

10 

c0t 0 

ll 

4 

N s,. ~~.., ..... u .. 40 '•· lli•illl"'' 

........ 3 30 

c. 

., 2 ... 20 

-........ 10 10 

>-.. 0 - 0 0 

., 4 c A. •••••••• 40 40 x. ,, .. ,, ....... ., 

Cl 3 s.. ,.,,;., ... , 

30 30 

2 20 20 

10 10 

0 0 0 I. ereuhiulu 

1.0 1.0 

0.8 0.8 0 

0.6 -+J 0.6 

«J 

a: 0.4 0.4 

0.2 0.2 0.2 

0.0 

4 5 6 7 8 9 10 11 0.0 

4 5 6 7 8 9 10 11 1 2 3 4 5 6 789101112 

Month 

Figure 2. Seasonal trapping density (upper three diagrams in each column) and 

relative proportion of catch (lower diagram in each column) in three separate 

years for (A) the cerambycids: Honochamus alter.natus, Spondylis buprestoides, 

and Arhopalus coreanus, (B) the weevils: Shirahoshizo rufescens, S. pini, and 

S. insidiosus, and (C) the scolytids: Taenioglyptis fulvus, Tomicus 

piniperda, and Xylosandrus crassiusculus. 

Sh. rufescens was the first species to appear in the spring (Fig. 2B). The main season for Sh. 

insidiosus extended from May to July and showed several peaks during the flight period. 

Ta. fulvus was attracted to the a-pinene traps throughout the year (Fig. 2C). This species was 

able to repeat one or two generations under field conditions (Oda 1970). To. piniperda 

characteristically appeared in early spring, showing peaks from March to April. X crassiusculus showed 

two peaks, one from May to June and a second from September to October. 

399 
Local Changes 

The distribution of M. altematus was concentrated in an area between 1 and 3 km from the 

seashore, and that of A. coreanus in the inland portion of the ridge. Sp. buprestoides appeared both in 

coastal and inland areas. 

The number of Sh. pini increased with the distance from the seashore and attained maximal 

numbers at a point 6 to 8 km inland. Neither Sh. insidiosus nor Sh. rufescens showed such a 

regular/uniform/consistent increase. 

In the coastal region, Ta. fulvus was the dominant scolytid species. The ratio of Ta. fulvus 

exceeded 95 percent at the seashore, and that of To. piniperda increased with distance from the 

seashore. The main distribution area of X crassiusculus was 3 to 4 km from the seashore. 

Community Structure 

By the seasonal changes in diversity index (H'), local differences in community structure were 

analyzed. 

For the cerambycid beetle community, the study area was divided into the coastal portion and 

the inland portion at a point about 4 km from the seashore. For the weevil community, traps were 

divided into two groups by a borderline drawn at a point 2 to 3 km from the seashore. Traps were 

also grouped into two clusters for the scolytid beetle community and the boundary between the two 

groups was drawn at a point 3 to 4 km from the seashore. 

Points where the community structure of subcortical insects changed were found to overlap with 

alterations in elements of the pine stand structure such as tree height and species composition. Thus 

the structure of pine forests appears to affect the community structures of subcortical insects. 

SUMMARY 

In Japanese pine forests, 36, 59 and 52 species of cerambycid beetles, weevils, and scolytid 

beetles, respectively, were attracted to/by traps baited with a-pinene and ethyl alcohol over a period of 

3 years. For each group of insects, seasonal and spatial changes of dominant species were investigated. 

LITERATURE CITED 

HAYASHI, M., MORIMOTO, K., and KIMOTO, S. 1984. The Coleoptera of Japan in color. 6. 

Hoikusha Pub., Osaka. 438 p. (In Japanese.) 

NOBUCHI, A 1966. Studies on Scolytidae. IV. Bull. Gov. For. Exp. Stn. 185: 1-49. (In Japanese with 

English summary.) 

ODA, K. 1970. Pine borers in Japan, p. 415-438. Ringyo shin gijutsu 33 sen. (In Japanese.) 

SHIKOKU BRANCH GOV. FOR. EXP. STN. 1962. Pine borers in Shikoku Island. Kochi Rinyu 

429: 2-12, 430: 8-29, 431: 2-14, 432: 2-17, 433: 1-18. (In Japanese.) 

Y ASUNAGA, K. 1964. Pine beetles and their natural enemies. Rinya Kyosaikai, Kumamoto. 123 p. (In 

Japanese.) 

-It U.S. Government Prlnllng Office: 1991~1-151 400 
Baranchikov, Yuri N.; Mattson, William J.; Hain, Fred P.; Payne, 

Thomas L., eds. 1991. Forest Insect Guilds: Patterns of Interaction 

with Host Trees; 1989 August 13-17; Abakan, Siberia, U.S.S.R. Gen. 

Tech. Rep. NE-153. Radnor, PA: U.S. Department of Agriculture, 

Forest Service, Northeastern Forest Experiment Station. 400 p. 

Twenty-five full-length papers and 19 poster papers on the interactions 

of different forest insect guilds with their host plants are presented in 

this proceedings, which is the result of an International Union of 

Forestry Research Organization Symposium that took place in Abakan, 

Siberia, U.S.S.R. in August 1989. 
Headquarters of the Northeastern Forest Experiment Station Is In Radnor, Penn· 

sylvania. Field laboratories are maintained at: 

Amherst, Massachusetts, In cooperation with the University of Massachusetts 

Burlington, Vermont, In cooperation with the University of Vermont 

Delaware, Ohio 

Durham, New Hampshire, In cooperation with the University of New Hampshire 

Hamden, Connecticut, In cooperation with Yale University 

Morgantown, West VIrginia, In cooperation with West VIrginia University 

Orono, Maine, In cooperation with the University of Maine 

Parsons, West VIrginia 

Princeton, West VIrginia 

Syracuse, New York, In cooperation with the State UniversHy of New York, 

College of Environmental Sciences and Forestry at Syracuse University 

University Park, Pennsylvania, In cooperation with The Pennsylvania State Unl· 

verslty 

Warren, Pennsylvania 

Persons of any race, color, national origin, sex, age, religion, or with any handicapping condition are welcome to use and enjoy all facilities, programs, and services of 

the USDA. Discrimination in any form is strictly against agency policy, and should be 

reported to the Secretary of Agriculture, Washington, DC 20250. 

•caring for the Land and Serving People Through Research•