Herbivore offense

Annual Review of Ecology and Systematics

Volumn 33, Issue , 2002, Pages 641-664

  Karban, Richard ^a   Agrawal, Anurag A ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Choice; Coevolution; Enzymatic metabolism; Plant herbivore interactions; Preference performance correlation; Sequestration

Indexed keywords

COEVOLUTION; PLANT-HERBIVORE INTERACTION;

ANIMALIA;

EID: 0036909585     PISSN: 00664162     EISSN: None     Source Type: Journal    
DOI: 10.1146/annurev.ecolsys.33.010802.150443     Document Type: Review

References (143)

1. Agrawal AA. 2001. Phenotypic plasticity in the interactions and evolution of species. Science 294:321-26
2. Agrawal AA, Kobayashi C, Thaler JS. 1999. Influence of prey availability and induced host-plant resistance on omnivory by western flower thrips. Ecology 80:518-23
3. Agrawal AA, Vala F, Sabelis MW. 2002. Induction of preference and performance after acclimation to novel hosts in a phytophagous spider mite: Adaptive plasticity? Am. Nat. 159:553-65
4. Appel HM, Martin MM. 1992. Significance of metabolic load in the evolution of host specificity of Manduca sexta. Ecology 73:216-28
5. Arms K, Feeny P, Lederhouse RC. 1974. Sodium: Stimulus for puddling behavior by tiger swallowtail butterflies. Papilio Glaucus. Science 185:372-74
6. Beck J, Muhlenberg E, Fiedler K. 1999. Mudpuddling behavior in tropical butterflies: In search of proteins or minerals? Oecologia 119:140-48
7. Berenbaum MR. 1987. Charge of the light brigade: Phototoxicity as a defense against insects. In Light-Activated Pesticides, ed. JR Heitz, KR Downum, pp. 206-16. Washington, DC: Am. Chem. Soc.
8. Berenbaum MR, Zangerl AR. 1994. Costs of inducible defense: Protein limitation, growth, and detoxification in parsnip webworms. Ecology 75:2311-17
9. Bernays EA. 1986. Diet-induced head allometry among foliage-chewing insects and its importance for graminivores. Science 231:495-97
10. Bernays EA, ed. 1990. Insect-Plant Interactions. Vol. II, Boca Raton, FL: CRC
11. Bernays EA. 1991. Evolution of insect morphology in relation to plants. Philos. Trans. R. Soc. London Ser. B 333:257-64
12. Bernays EA. 1993. Aversion learning and feeding. In Insect Learning. Ecological and Evolutionary Perspectives, ed. DR Papay, AC Lewis, pp. 1-17. New York: Chapman & Hall
13. Bernays EA. 2001. Neural limitations in phytophagous insects: Implications for diet breadth and evolution of host affiliation. Annu. Rev. Entomol. 46:703-27
14. Bernays EA, Bright KL, Gonzalez N, Angel J. 1994. Dietary mixing in a generalist herbivore: Tests of two hypotheses. Ecology 75:1997-2006
15. Bernays EA, Graham M. 1988. On the evolution of host specificity in phytophagous arthropods. Ecology 69:886-92
16. Bernays EA, Janzen DH. 1988. Saturniid and sphingid caterpillars: Two ways to eat leaves. Ecology 69:1153-60
17. Bernays EA, Lee JC. 1988. Food aversion learning in the polyphagous grasshopper Schistocerca americana. Physiol. Entomol. 13:131-37
18. Bjorndal KA. 1991. Diet mixing: Nonadditive interactions of diet items in an omnivorous freshwater turtle. Ecology 72:1234-41
19. Blua MJ, Perring TM, Madore MA. 1994. Plant virus-induced changes in aphid population development and temporal fluctuations in plant nutrients. J. Chem. Ecol. 20:691-707
20. Blum MS, Severson RF, Arrendale RF, Whitman DW, Escoubas P, et al. 1990. A generalist herbivore in specialist mode. Metabolic sequestrative, and defensive consequences. J. Chem. Ecol. 16:223-44
21. Bolter CJ, Jongsma MA. 1995. Colorado potato beetles (Leptinotarsa decemlineata) adapt to proteinase inhibitors induced in potato leaves by methyl jasmonate. J. Insect Physiol. 41:1071-78
22. Bowers MD. 1992. The evolution of unpalatability and the costs of chemical defense in insects. In Insect Chemical Ecology, ed. BD Roitberg, MB Isman, pp. 216-44. New York, Chapman & Hall
23. Brattsten LB. 1988. Exzymatic adaptation in leaf-feeding insects to host-plant allelochemicals. J. Chem. Ecol. 14:1919-40
24. Breton LM, Addicott JF. 1992. Density-dependent mutualism in an aphid-ant interaction. Ecology 73:2175-80
25. Broadway RM. 1995. Are insects resistant to plant proteinase inhibitors? J. Insect Physiol. 41:107-16
26. Broadway RM. 1997. Dietary regulation of serine proteinases that are resistant to serine proteinase inhibitors. J. Insect Physiol. 43:855-74
27. Buchner P. 1965. Endosymbiosis of Animals with Plant Microorganisms. New York: Intersci. 909 pp.
28. Camara MD. 1997. Physiological mechanisms underlying the costs of chemical defence in Junonia coenia Hubner (Nymphalidae): A gravimetric and quantitative genetic analysis. Evol. Ecol. 11:451-69
29. Carroll SP, Boyd C. 1992. Host race radiation in the soapberry bug: Natural history with the history. Evolution 46:1052-69
30. Carroll SP, Dingle H, Klassen SP. 1997. Genetic differentiation of fitness-associated traits among rapidly evolving populations of the soapberry bug. Evolution 51:1182-88
31. Carroll SP, Klassen SP, Dingle H. 1998. Rapidly evolving adaptations to host ecology and nutrition in the soapberry bug. Evol. Ecol. 12:955-68
32. Chen DQ, Montlor CB, Purcell AH. 2000. Fitness effects of two facultative endosymbiotic bacteria on the pea aphid. Acyrthosiphon pisum, and the blue alfalfa aphid, A. kondoi. Entomol. Exp. Appl. 95:315-23
33. Cloutier C, Jean C, Fournier M, Yelle S, Michaud D. 2000. Adult Colorado potato beetles, Leptinotarsa decemlineata compensate for nutritional stress on oryzacystatin I-transgenic potato plants by hypertrophic behavior and over-production of insensitive proteases. Arch. Insect Biochem. Physiol. 44:69-81
34. Cornell HV. 1983. The secondary chemistry and complex morphology of galls formed by the Cynipinae (Hymenoptera): Why and how? Am. Midl. Nat. 110:225-34
35. Crespi B, Worobey M. 1998. Comparative analysis of gall morphology in Australian gall thrips: The evolution of extended phenotypes. Evolution 52:1686-96
36. Currie CR, Scott JA, Summerbell RC, Malloch D. 1999. Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398:701-4
37. Dearing MD. 1997. The manipulation of plant toxins by a food-hoarding herbivore. Ochotona princeps. Ecology 78:774-81
38. Denno RF, Benrey B. 1997. Aggregation facilitates larval growth in the neotropical nymphalid butterfly Chlosyne janais. Ecol. Entomol. 22:133-41
39. Detling JK, Dyer MI. 1981. Evidence for potential plant growth regulators in grasshoppers. Ecology 62:485-88
40. Dobler S. 2001. Evolutionary aspects of defense by recycled plant compounds in herbivorous insects. Basic Appl. Ecol. 2:15-26
41. Douglas AE. 1998. Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. Annu. Rev. Entomol. 43:17-37
42. Dowd P. 1991. Symbiont-mediated detoxification in insect herbivores. In Microbial Mediation of Plant-Herbivore Interactions, ed. P Barbosa, VA Krischik, C Jones, pp. 411-40. New York: Wiley
43. Duffey SS. 1980. Sequestration of plant natural-products by insects. Annu. Rev. Entomol. 25:447-77
44. Duffey SS, Stout MJ. 1996. Antinutritive and toxic components of plant defense against insects. Arch. Insect Biochem. Physiol. 32:3-37
45. Dukas R, Bernays EA. 2000. Learning improves growth rate in grasshoppers. Proc. Natl. Acad. Sci. USA 97:2637-40
46. Dussourd DE. 1993. Foraging with finesse: Caterpillar adaptations for circumventing plant defenses. In Caterpillars: Ecological and Evolutionary Constraints on Foraging, ed. NE Stamp, TM Casey, pp. 92-131. New York: Chapman & Hall
47. Dussourd DE. 1999. Behavioral sabotage of plant defense: Do vein cuts and trenches reduce insect exposure to exudates? J. Insect Behav. 12:501-15
48. Dussourd DE, Denno RF. 1991. Deactivation of plant defense: Correspondence between insect behavior and secretory canal architecture. Ecology 72:1383-96
49. Dussourd DE, Denno RF. 1994. Host range of generalist caterpillars: Trenching permits feeding on plants with secretory canals. Ecology 75:69-78
50. Dyer LA. 1995. Tasty generalists and nasty specialists? Antipredator mechanisms in tropical lepidoptera larvae. Ecology 76:1483-96
51. Dyer LA, Gentry G. 1999. Predicting natural-enemy responses to herbivores in natural and managed systems. Ecol. Appl. 9:402-8
52. Dyer MI. 2000. Herbivores, biochemical messengers and plants: Aspects of intertrophic transduction. In Invertebrates as Webmasters in Ecosystems, ed. DC Coleman, PF Hendrix, pp. 115-40. Wallingford, UK: CABI
53. Dyer MI, Moon AM, Brown MR, Crossley DA. 1995. Grasshopper crop and midgut extract effects on plants: An example of reward feedback. Proc. Natl. Acad. Sci. USA 92:5475-78
54. Endler JA. 1986. Natural Selection in the Wild. Princeton NJ: Princeton Univ. Press. 336 pp.
55. Engler HS, Spencer KC, Gilbert LE. 2000. Insect metabolism - Preventing cyanide release from leaves. Nature 406:144-45
56. Felton GW, Eichenseer H. 1999. Herbivore saliva and its effect on plant defense against herbivores and pathogens. In Induced Plant Defenses Against Pathogens and Herbivores, ed. AA Agrawal, S Tuzun, E Bent, pp. 19-36. St. Paul, MN: Am. Phytopathol. Soc.
57. Felton GW, Korth KL, Bi JL, Wesley SV, Huhman DV, et al. 1999. Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Curr. Biol. 9:317-20
58. Fereres A, Lister RM, Araya JE, Foster JE. 1989. Development and reproduction of the English grain aphid (Homoptera: Aphididae) on wheat cultivars infected with barley yellow dwarf virus. Environ. Entomol. 18:388-93
59. Feyereisen R. 1999. Insect P450 enzymes. Annu. Rev. Entomol. 44:507-33
60. Fisher M. 1987. The effect of previously infested spruce needles on the growth of the green spruce aphid, Elatobium abietinum, and the effect of the aphid on the amino acid balance of the host plant. Ann. Appl. Biol. 111:33-41
61. Fox CW. 1993. A quantitative genetic analysis of oviposition preference and larval performance on two hosts in the bruchid beetle. Callosobruchus maculatus. Evolution 47:166-75
62. Fox CW, Thakar KJ, Mousseau TA. 1997. Egg size plasticity in a seed beetle: An adaptive maternal effect. Am. Nat. 149:149-63
63. Fox L. 1975. Cannibalism in natural populations. Annu. Rev. Ecol. Syst. 6:87-106
64. Freeland WJ, Janzen DH. 1974. Strategies in herbivory by mammals: The role of plant secondary compounds. Am. Nat. 108:269-89
65. Furuta K. 1986. Host preference and population dynamics in an autumnal population of the maple aphid. Periphyllus californiensis Shinji (Homoptera, Aphididae). J. Appl. Entomol. 102:93-100
66. Hagele BF, Rowell-Rahier M. 1999. Dietary mixing in three generalist herbivores: Nutrient complementation or toxin dilution? Oecologia 119:521-33
67. Hagen RH, Chabot JF. 1986. Leaf anatomy of maples (Acer) and host use by Lepidoptera larvae. Oikos 47:335-45
68. Hamilton WD, Brown SP. 2001. Autumn tree colours as a handicap signal. Proc. R. Soc. London Ser. B 268:1489-93
69. Hay ME, Duffy JE, Fenical W. 1990. Host-plant specialization decreases predation on a marine amphipod: An herbivore in plant's clothing. Ecology 71:733-43
70. Heath IB. 1988. Gut fungi. TREE 3:167-71
71. Holldobler B, Wilson EO. 1990. The Ants. Cambridge MA: Harvard Univ. Press. 732 pp.
72. Hulley PE. 1988. Caterpillar attacks plant mechanical defence by mowing trichomes before feeding. Ecol. Entomol. 13:239-41
73. Jaenike J. 1989. Genetic population structure of Drosophila tripunctata: Patterns of variation and covariation of traits affecting resource use. Evolution 43:1467-82
74. Jones CG. 1984. Microorganisms as mediators of plant resource exploitation by insect herbivores. In A New Ecology: Novel Approaches to Interactive Systems, ed. PW Price, CN Slobodchikoff, WS Gaud, pp. 53-99. New York: Wiley
75. Jongsma MA, Bakker PL, Peters J, Bosch D, Stiekema WJ. 1995. Adaptation of Spodoptera exigua larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proc. Natl. Acad. Sci. USA 92:8041-45
76. Karban R, Agrawal AA, Mangel M. 1997. The benefits of induced defenses against herbivores. Ecology 78:1351-55
77. Karban R, Agrawal AA, Thaler JS, Adler LS. 1999. Induced plant responses and information content about risk of herbivory. TREE 14:443-47
78. Karban R, Baldwin IT. 1997. Induced Responses to Herbivory. Chicago, IL: Univ. Chicago Press. 319 pp.
79. Karban R, Courtney S. 1987. Intraspecific host plant choice: Lack of consequences for Streptanthus tortuosus (Cruciferae) and Eucloe hyantis (Lepidoptera: Pieridae). Oikos 48:243-48
80. Klepzig KD, Smalley EB, Raffa KF. 1996. Combined chemical defenses against an insect-fungal complex. J. Chem. Ecol. 22:1367-88
81. Labandeira CC. 1997. Insect mouthparts: Ascertaining the paleobiology of insect feeding strategies. Annu. Rev. Ecol. Syst. 28:153-93
82. Larson KC, Whitham TG, 1991. Manipulation of food resources by a gall-forming aphid: The physiology of sink-source interactions. Oecologia 88:15-21
83. Leschine SB. 1995. Cellulose degradation in anaerobic environments. Annu. Rev. Microbiol. 49:399-426
84. Levins R. 1968. Evolution in Changing Environments. Princeton, NJ: Princeton Univ. Press
85. Llewwllyn M. 1982. The energy economy of fluid feeding herbivorous insects. In International Symposium on Insect-Plant Relationships, Proc. 5th Int. Syrup. Insect-Plant Relationships, ed. JH Viller, AK Minks, pp. 243-51. Wageningen: Cent. Agric. Publ. Doc.
86. Lopez ER, Van Driesche RG, Elkinton JS. 1989. Influence of group size on daily per capita birth rates of the cabbage aphid (Homoptera: Aphididae) on collards. Environ. Entomol. 18:1086-89
87. Mattson WJ. 1980. Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst. 11:119-61
88. Mayhew PJ. 1997. Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79:417-28
89. Mayhew PJ. 2001. Herbivore host choice and optimal bad motherhood. TREE 16:165-67
90. Miles PW. 1990. Aphid salivary secretions and their involvement in plant toxicoses. In Aphid-Plant Genotype Interactions, ed. RK Campbell, RD Eikenbary, pp. 131-47. Amsterdam: Elsevier
91. Mullin C, Croft B. 1983. Host-related alterations of detoxification enzymes in Tetranychus urticae (Acari: Tetranychidae). Environ. Entomol. 12:1278-82
92. Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, et al. 2002. Herbivory: Caterpillar saliva beats plant defense - A new weapon emerges in the evolutionary arms race between plants and herbivores. Nature 416:599-600
93. Neal JJ. 1987. Metabolic costs of mixed-function oxidase induction in Heliothis zea. Entomol. Exp. Appl. 43:175-79
94. Nebeker TE, Hodges JD, Blanche CA. 1993. Host response to bark beetle and pathogen colonization. In Beetle-Pathogen Interactions in Conifer Forests, ed. T Schowalter, G Filip, pp. 157-73. New York, Academic
95. Nyman T, Julkunen-Tiitto R. 2000. Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc. Natl. Acad. Sci. USA 97:13184-87
96. Nyman T, Widmer A, Roinnen H. 2000. Evolution of gall morphology and host-plant relationships in willow-feeding sawflies (Hymenoptera: Tenthredinidae). Evolution 54:526-33
97. Papaj DR, Prokopy RJ. 1989. Ecological and evolutionary aspects of learning in phytophagous insects. Annu. Rev. Entomol. 34:315-50
98. Pennings SC, Nadeau MT, Paul VJ. 1993. Selectivity and growth of the generalist herbivore Dolabella auricularia feeding upon complimentary resources. Ecology 74:879-90
99. Pennings SC, Paul VJ. 1993. Sequestration of dietary secondary metabolites by three species of sea hares - Location, specificity and dynamics. Marine Biol. 117:535-46
100. Pires CSS, Price PW, Fontes EG. 2000. Preference-performance linkage in the neotropical spittlebug Deois flavopicta, and its relation to the phylogenetic constraints hypothesis. Ecol. Entomol. 25:71-80
101. Preston CA, Lewandowski C, Enyedi AJ, Baldwin IT. 1999. Tobacco mosaic virus inoculation inhibits wound-induced jasmonic acid-mediated responses within but not between plants. Planta 209:87-95
102. Price PW. 1992. Plant resources as the mechanistic basis for insect herbivore population dynamics. In Effects of Resource Distribution on Animal-Plant Interactions, ed. MD Hunter, T Ohgushi, PW Price, pp. 139-73. San Diego: Academic
103. Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE. 1980. Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11:41-65
104. Price PW, Cobb N, Craig TP, Fernandes GW, Itami JK, et al. 1990. Insect Herbivore Population Dynamics on Trees and Shrubs: New Approaches Relevant to Latent and Eruptive Species and Life Table Development. See Bernays 1990, pp. 1-38
105. Price PW, Fernandes GW, Waring GL. 1987. Adaptive nature of insect galls. Environ. Entomol 16:15-24
106. Pulliam HR. 1975. Diet optimization with nutrient constraints. Am. Nat. 109:765-68
107. Rank NE, Kopf A, Julkunen-Tiitto R, Tahvanainen J. 1998. Host preference and larval performance of the salicylate-using leaf beetle Phratora vitellinae. Ecology 79:618-31
108. Rathcke BJ, Poole RW. 1975. Coevolutionary race continues: Butterfly larval adaptation to plant trichomes. Science 187:175-76
109. Raupp MJ. 1985. Effects of leaf toughness on mandibular wear of the leaf beetle. Plagiodera versicolora. Ecol. Entomol. 10:73-80
110. Reeve HK, Sherman PW. 2001. Optimality and phylogeny: A critique of current thought. In Adaptation and Optimality, ed. SH Orzack, E Sober, pp. 64-113. Cambridge, UK: Cambridge Univ. Press
111. Reznick D, Travis J. 1996. The empirical study of adaptation in natural populations. In Adaptation, ed. MR Rose, GV Lander, pp. 243-89. San Diego, CA: Academic
112. Rhoades DF. 1985. Offensive-defensive interactions between herbivores and plants: Their relevance in herbivore population dynamics and ecological theory. Am. Nat. 125:205-38
113. Rosenthal GA, Dahlman DL, Janzen DH. 1978. L-canaline detoxification: A seed predator's biochemical mechanism. Science 202:528-29
114. Rosenthal GA, Hughes CG, Janzen DH. 1982. L-canavanine, a dietary nitrogen source for the seed predator Caryedes brasiliensis (Bruchidae). Science 217:353-55
115. Ryan CA. 1990. Proteinase inhibitors in plants: Genes for improving defenses against insects and pathogens. Annu. Rev. Phytopathol. 28:425-49
116. Sagers CL. 1992. Manipulation of host plant quality: Herbivores keep leaves in the dark. Funct. Ecol. 6:741-43
117. Sandberg SL, Berenbaum MR. 1989. Leaf-tying by tortricid larvae as an adaptation for feeding on phototoxic Hypericum perforatum. J. Chem. Ecol. 15:875-85
118. Scheirs J, De Bruyn L, Verhagen R. 2000. Optimization of adult performance determines host choice in a grass miner. Proc. R. Soc. London Ser. B 267:2065-69
119. Simpson SJ, Simpson CL. 1990. The Mechanisms of Nutritional Compensation by Phytophagous Insects. See Bernays 1990, pp. 111-60
120. Simpson SJ, White PR. 1990. Associative learning and locust feeding: Evidence for a 'learned hunger' for protein. Anim. Behav. 40:506-13
121. Singer MC, Ng D, Thomas CD. 1988. Heritability of oviposition preference and its relationship to offspring performance within a single insect population. Evolution 42:977-85
122. Slansky F. 1993. Nutritional Ecology: The Fundamental Quest for Nutrients. See Stamp & Casey 1993, pp. 29-91
123. Snyder MJ, Glendinning JI. 1996. Causal connection between detoxification enzyme activity and consumption of a toxic plant compound. J. Comp. Physiol. A 179:255-61
124. Stachowicz JJ, Hay ME. 1999. Reducing predation through chemically mediated camouflage: Indirect effects of plant defenses on herbivores. Ecology 80:495-509
125. Stamp NE, Casey TM, eds. 1993. Ecological and Evolutionary Constraints on Foraging. New York: Chapman & Hall
126. Thaler JS, Fidantsef AL, Duffey SS, Bostock RM. 1999. Trade-offs in plant defense against pathogens and herbivores: A field demonstration of chemical elicitors of induced resistance. J. Chem. Ecol. 25:1597-1609
127. Thompson DB. 1992. Consumption rates and the evolution of diet-induced plasticity in the head morphology of Melanoplus femurrubrum (Othoptera: Acrididae). Oecologia 89:204-13
128. Thompson DB. 1999. Genotype-environment interaction and the ontogeny of diet-induced phenotypic plasticity in size and shape of Melanoplus femurrubrum (Orthoptera: Acrididae). J. Evol. Biol. 12:38-48
129. Thompson JN. 1988. Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Ent. Exp. Appl. 47:3-14
130. Thompson JN, Pellmyr O. 1991. Evolution of oviposition behavior and host preference in Lepidoptera. Annu. Rev. Entomol. 36:65-89
131. Vander Wall SB. 1990. Food Hoarding in Animals. Chicago: Univ. Chicago Press. 445 pp.
132. Via S. 1999. Cannibalism facilitates the use of a novel environment in the flour beetle. Tribolium castaneum. Heredity 82:267-75
133. Waldbauer GP, Fraenkel G. 1961. Feeding on normally rejected plants by maxillectomized larvae of the tobacco hornworm. Protoparce Sexta (Johan.) Ann. Ent. Soc. Am. 54:477-85
134. Waldbauer GP, Friedman S. 1991. Self-selection of optimal diets by insects. Annu. Rev. Entomol. 36:43-63
135. Way MJ, Cammell M. 1970. Aggregation behaviour in relation to food utilization by aphids. In Animal Populations in Relation to Their Food Resources, ed. A Watson, pp. 229-47. Oxford: Blackwell
136. Weis AE, Kapelinski A. 1994. Variable selection on Eurosta's gall size. II. A path analysis of the ecological factors behind selection. Evolution 48:734-45
137. Whitham TG. 1978. Habitat selection by Pemphigus aphids in response to resource limitation and competition. Ecology 59:1164-76
138. Whitham TG. 1980. The theory of habitat selection: Examined and extended using Pemphigus aphids. Am. Nat. 115:449-66
139. Whitney HS. 1982. Relationships between bark beetles and symbiotic organisms. In Bark Beetles in North American Conifers, ed. JB Mitton, KB Sturgeon, pp. 183-211. Austin, TX: Univ. Texas Press
140. Williams AG, Whitham TG. 1986. Premature leaf abscission: An induced plant defense against gall aphids. Ecology 67:1619-27
141. Wilson EO. 1975. Sociobiology. Cambridge MA: Harvard Univ. Press. 697 pp.
142. Zalucki MP, Clarke AR, Malcolm SB. 2002. Ecology and behavior of first instar larval lepidoptera. Annu. Rev. Entomol. 47:361-93
143. Zangerl AR, Bazzaz FA. 1992. Theory and pattern in plant defense allocation. In Plant Resistance to Herbivores and Pathogens, ed. RS Fritz, EL Simms, pp. 363-91. Chicago: Univ. Chicago Press