Cascading effects of host size and host plant species on parasitoid resource allocation

Ecological Entomology

Volumn 36, Issue 6, 2011, Pages 724-735

  Stoepler, Teresa M ^a   Lill, John T ^a   Murphy, Shannon M ^b  

^a GEORGE WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF DENVER   (United States)

Author keywords

Bottom up; Braconidae; Eulophidae; Herbivore; Host choice; Limacodidae; Stage specific parasitism; Tachinidae; Tritrophic interactions

Indexed keywords

BOTTOM-UP APPROACH; CATERPILLAR; FLY; FORAGING BEHAVIOR; GROWTH; HERBIVORE; HOST PLANT; HOST-PARASITOID INTERACTION; NATURAL ENEMY; OVIPOSITION; PARASITISM; PHENOLOGY; REARING; RESEARCH WORK; RESOURCE ALLOCATION; SEX ALLOCATION; SPECIALIZATION; TROPHIC LEVEL; WASP;

BRACONIDAE; EULOPHIDAE; HEXAPODA; LIMACODIDAE; MEGASCOLIA FLAVIFRONS; TACHINIDAE;

EID: 81855211008     PISSN: 03076946     EISSN: 13652311     Source Type: Journal    
DOI: 10.1111/j.1365-2311.2011.01322.x     Document Type: Article

References (90)

1. Adamo, S.A., Robert, D., Perez, J. & Hoy, R.R. (1995) The response of an insect parasitoid, Ormia ocheacea (Tachinidae), to the uncertainty of larval success during infestation. Behavioral Ecology and Sociobiology, 36, 111-118.
2. Alcock, J. & Kemp, D. (2006) The hilltopping mating system of Leschenaultia adusta (Loew) (Diptera: Tachinidae). Journal of Insect Behavior, 19, 645-656.
3. Allen, G.R. & Hunt, J. (2001) Larval competition, adult fitness, and reproductive strategies in the acoustically orienting ormiine Homotrixa alleni (Diptera: Tachinidae). Journal of Insect Behavior, 14, 283-297.
4. Askew, R.R. & Shaw, M.R. (1986) Parasitoid communities: their size, structure and development. Insect Parasitoids (ed. by J. Waage and D. Greathead), pp. 225-264. Academic Press, London, U.K.
5. Awmack, C.S. & Leather, S.R. (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology, 47, 817-844.
6. Barbosa, P. & Greenblatt, J. (1979) Suitability, digestibility and assimilation of various host plants of the gypsy moth Lymantria dispar L. Oecologia, 43, 111-119.
7. Barbosa, P., Gross, P. & Kemper, J. (1991) Influence of plant allelochemicals on the tobacco hornworm and its parasitoid, Cotesia congregata. Ecology, 72, 1567-1575.
8. Barbosa, P., Saunders, J.A., Kemper, J., Trumble, R., Olechno, J. & Martinat, P. (1986) Plant allelochemicals and insect parasitoids: effects of nicotine on Cotesia congregata (Say) (Hymenoptera: Braconidae) and Hyposoter annulipes (Cressen) (Hymenoptera: Ichneumonidae). Journal of Chemical Ecology, 12, 1319-1328.
9. Belshaw, R. (1994) Life history characteristics of Tachinidae (Diptera) and their effect on polyphagy. Parasitoid Community Ecology (ed. by W. Hawkins and B. A. Sheehan), pp. 145-162. Oxford University Press, Oxford, U.K.
10. Blüthgen, N., Menzel, F. & Blüthgen, N. (2006) Measuring specialization in species interaction networks. BioMed Central Ecology, 6, 9.
11. Blüthgen, N., Menzel, F., Hovestadt, T., Fiala, B. & Blüthgen, N. (2007) Specialization, constraints, and conflicting interests in mutualistic networks. Current Biology, 17, 341-346.
12. Bokonon-Ganta, A.H., Van Alphen, J.J.M. & Neuenschwander, P. (1996) Competition between Gyranusoidea tebygi and Anagyrus mangicola, parasitoids of the mango mealybug, Rastrococcus invadens: interspecific host discrimination and larval competition. Entomologia Experimentalis et Applicata, 79, 179-185.
13. Bowers, M.D. (2003) Host plant suitability and defensive chemistry of the Catalpa sphinx, Ceratomia catalpae. Journal of Chemical Ecology, 29, 2359-2367.
14. Briggs, C.J. (1993) Competition among parasitoid species on a stage-structured host and its effect on host suppression. American Naturalist, 141, 372-397.
15. Brodeur, J. & Vet, L.E.M. (1995) Relationships between parasitoid host-range and host-defense - a comparative study of egg encapsulation in two related parasitoid species. Physiological Entomology, 20, 7-12.
16. Bukovinszky, T., Poelman, E.H., Gols, R., Prekatsakis, G., Vet, L.E.M., Harvey, J.A. et al. (2009) Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism. Oecologia, 160, 299-308.
17. Campan, E.D.M., Callejas, A., Rahier, M. & Benrey, B. (2005) Interpopulation variation in a larval parasitoid of bruchids, Stenocorse bruchivora (Hymenoptera: Braconidae): host plant effects. Environmental Entomology, 34, 457-465.
18. Campbell, B.C. & Duffey, S.F. (1979) Tomatine and parasitic wasps: potential incompatibility of plant antibiosis with biological control. Science, 205, 700-702.
19. Caron, V., Myers, J.H. & Gillespie, D.R. (2008) Fitness-related traits in a parasitoid fly are mediated by effects of plants on its host. Journal of Applied Entomology, 132, 663-667.
20. Caron, V., Myers, J.H. & Gillespie, D.R. (2010) The failure to discriminate: superparasitism of Trichoplusia ni Hubner by a generalist tachinid parasitoid. Bulletin of Entomological Research, 100, 255-261.
21. Charnov, E.L. (1982) The Theory of Sex Allocation. Princeton University Press, Princeton, New Jersey.
22. Charnov, E.L. & Skinner, S.W. (1985) Complementary approaches to the understanding of parasitoid oviposition decisions. Environmental Entomology, 14, 383-391.
23. Charnov, E.L., Los-den Hartogh, Z.L., Jones, W.T. & van den Assem, J. (1981) Sex ratio evolution in a variable environment. Nature, 289, 27-33.
24. Croft, P. & Copland, M. (1995) The effect of host instar on the size and sex ratio of the endoparasitoid Dacnusa sibirica. Entomologia Experimentalis et Applicata, 74, 121-124.
25. Dyar, H.G. (1890) The number of molts of lepidopterous larvae. Psyche, 5, 420-422.
26. Fidgen, J.G., Eveleigh, E.S. & Quiring, D.T. (2000) Influence of host size on oviposition behaviour and fitness of Elachertus cacoeciae attacking a low-density population of spruce budworm Choristoneura fumiferana larvae. Ecological Entomology, 25, 156-164.
27. Gates, M.W., Lill, J.T., Kula, R.R., O'Hara, J.E., Smith, D.R., Whitfield, J.B. et al. (2012) Review of parasitoid wasps and flies (Hymenoptera, Diptera) associated with Limacodidae (Lepidoptera) in North America, with a key to genera. Proceedings of the Entomological Society of Washington, in press.
28. Gentry, G.L. & Dyer, L.A. (2002) On the conditional nature of neotropical caterpillar defenses against their natural enemies. Ecology, 83, 3108-3119.
29. Godfray, H.C.J. (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, New Jersey.
30. Gols, R., Bukovinszky, T., van Dam, N.M., Dicke, M., Bullock, J.M. & Harvey, J.A. (2008) Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations. Journal of Chemical Ecology, 34, 132-143.
31. Gross, H.R., Rogers, C.E. & Carpenter, J.E. (1996) Development of Archytas marmoratus (Diptera: Tachinidae) reared in Galleria mellonella larvae (Lepidoptera: Pyralidae) feeding on selected diets. Biological Control, 6, 158-163.
32. Hågver, E.B. (1988) Multiparasitism of the green peach aphid, Myzus persicae: competition in the egg stage between Aphidius matricariae and Ephedrus cerasicola. Entomologia Experimentalis et Applicata, 47, 275-282.
33. Harvey, J.A. (1996) Venturia canescens parasitizing Galleria mellonella and Anagasta kuehniella: is the parasitoid a conformer or regulator? Journal of Insect Physiology, 42, 1017-1025.
34. Harvey, J.A. (2005) Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity. Entomologia Experimentalis et Applicata, 117, 1-13.
35. Harvey, J.A. & Vet, L.E.M. (1997) Venturia canescens parasitizing Galleria mellonella and Anagasta kuehniella; differing suitability of two hosts with highly variable growth potential. Entomologia Experimentalis et Applicata, 84, 93-100.
36. Harvey, J.A., Harvey, I.F. & Thompson, D.J. (1994) Flexible larval growth allows use of a range of host sizes by a parasitoid wasp. Ecology, 75, 1420-1428.
37. Harvey, J.A., Bezemer, T.M., Elzinga, J.A. & Strand, M.R. (2004) Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size. Ecological Entomology, 29, 35-43.
38. Heimpel, G.E. & de Boer, J.G. (2008) Sex determination in the Hymenoptera. Annual Review of Entomology, 53, 209-30.
39. Henry, L.M., May, N., Acheampong, S., Gillespie, D.R. & Roitberg, B.D. (2010) Host-adapted parasitoids in biological control: does source matter? Ecological Applications, 20, 242-250.
40. 3, and plant genotype. Oecologia, 137, 233-244.
41. Jones, W.T. (1982) Sex ratio and host size in a parasitoid wasp. Behavioral Ecology and Sociobiology, 10, 207-210.
42. Kato, M. (1994) Structure, organization, and response of a species-rich parasitoid community to host leafminer population dynamics. Oecologia, 97, 17-25.
43. King, B.H. (1987) Offspring sex ratios in parasitoid wasps. Quarterly Review of Biology, 62, 367-396.
44. King, B.H. (1989) Host-size-dependent sex-ratios among parasitoid wasps - does host growth matter? Oecologia, 78, 420-426.
45. King, B.H. & Napoleon, M.E. (2006) Using effects of parasitoid size on fitness to test a host quality model assumption with the parasitoid wasp Spalangia endius. Canadian Journal of Zoology - Revue Canadienne De Zoologie, 84, 1678-1682.
46. Kouamé, K.L. & Mackauer, M. (1991) Influence of aphid size, age and behaviour on host choice by the parasitoid wasp Ephedrus californicus: A test of host-size models. Oecologia, 88, 197-203.
47. Kula, R.R., Lill, J.T., Murphy, S.M. & Stoepler, T. (2009) First host records for the nearctic species Triraphis discoideus (Hymenoptera: Braconidae: Rogadinae). Entomological News, 120, 380-386.
48. Lampert, E.C. & Bowers, M.D. (2010) Host-plant species affects the quality of the generalist Trichoplusia ni as a host for the polyembryonic parasitoid Copidosoma floridanum. Entomologia Experimentalis et Applicata, 134, 287-295.
49. Lampson, L.J., Morse, J.G. & Luck, R.F. (1996) Host selection, sex allocation, and host feeding by Metaphycus helvolus (Hymenoptera: Encyrtidae) on Saissetia oleae (Homoptera: Coccidae) and its effect on parasitoid size, sex, and quality. Environmental Entomology, 25, 283-294.
50. Lederhouse, R.C., Morse, R.A., Ambrose, J.T., Burgett, D.M., Conner, W.E., Edwards, L. et al. (1976) Crepuscular mating aggregations in certain Ormia and Sitophaga. Annals of the Entomological Society of America, 69, 656-658.
51. Lee, J.H. & Pemberton, R.W. (2007) Seasonal phenology and stage-specific parasitism of the apple ermine moth, Yponomeuta malinellus Zeller, in Korea. Entomological Research, 37, 54-59.
52. Lee, K.P., Cory, J.S., Wilson, K., Raubenheimer, D. & Simpson, S.J. (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proceedings of the Royal Society B: Biological Sciences, 273, 823-829.
53. Li, B. & Mills, N. (2004) The influence of temperature on size as an indicator of host quality for the development of a solitary koinobiont parasitoid. Entomologia Experimentalis et Applicata, 110, 249-256.
54. Lill, J.T. (1999) Structure and dynamics of a parasitoid community attacking larvae of Psilocorsis quercicella (Lepidoptera: Oecophoridae). Environmental Entomology, 28, 1114-1123.
55. Lill, J.T. (2001) Selection on herbivore life-history traits by the first and third trophic levels: the devil and the deep blue sea revisited. Evolution, 55, 2236-2247.
56. Mackauer, M. & Sequeira, R. (1993) Patterns of development in insect parasites. Parasites and pathogens of insects (ed. by N. Beckage, S. N. Thompson and B. A. Federici), Vol. 1, pp. 1-23. Academic Press, New York, New York.
57. McLain, D.K., Marsh, N.B., Lopez, J.R. & Drawdy, J.A. (1990) Intravernal changes in the level of parasitization of the southern green stink bug (Hemiptera, Pentatomidae), by the feather-legged fly (Diptera, Tachinidae) - host sex, mating status, and body size as correlated factors. Journal of Entomological Science, 25, 501-509.
58. Murphy, S.M. (2007) The effect of host plant on larval survivorship of the Alaskan swallowtail butterfly (Papilio machaon aliaska). Entomologia Experimentalis et Applicata, 122, 109-115.
59. Murphy, S.M., Lill, J.T. & Smith, D.R. (2009) A scattershot approach to host location: uncovering the unique life history of the trigonalid hyperparasitoid Orthogonalys pulchella (Cresson). American Entomologist, 55, 82-87.
60. Murphy, S.M., Leahy, S.M., Williams, L.S. & Lill, J.T. (2010) Stinging spines protect slug caterpillars (Limacodidae) from multiple generalist predators. Behavioral Ecology, 21, 153-160.
61. Murphy, S.M., Lill, J.T. & Epstein, M.E. (2011) Natural history of limacodid moths (Zygaenoidea) in the environs of Washington, D.C. Journal of the Lepidopterists' Society, 65, 137-152.
62. Nakamura, S. (1995) Optimal clutch size for maximizing reproductive success in a parasitoid fly, Exorista japonica (Diptera: Tachinidae). Applied Entomology and Zoology, 30, 425-431.
63. Nicol, C.M.Y. & Mackauer, M. (1999) The scaling of body size and mass in a host-parasitoid association: influence of host species and stage. Entomologia Experimentalis et Applicata, 90, 83-92.
64. Ode, P.J. (2006) Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annual Review of Entomology, 51, 163-185.
65. Ojala, K., Julkunen-Tiitto, R., Lindstrom, L. & Mappes, J. (2005) Diet affects the immune defence and life-history traits of an Arctiid moth Parasemia plantaginis. Evolutionary Ecology Research, 7, 1153-1170.
66. Opitz, S.E.W. & Müller, C. (2009) Plant chemistry and insect sequestration. Chemoecology, 19, 117-154.
67. Parry, D. & Goyer, R.A. (2004) Variation in the suitability of host tree species for geographically discrete populations of forest tent caterpillar. Environmental Entomology, 33, 1477-1487.
68. Pintureau, B. & Grenier, S. (1992) Variability in morphological and biological characteristics in two strains of the parasitoid Lixophaga diatraeae (Diptera: Tachinidae). Biological Control, 2, 176-180.
69. Price, P.W. (1972) Parasitoids utilizing the same host: adaptive nature of differences in size and form. Ecology, 53, 190-195.
70. Rajapakse, C. & Walter, G. (2007) Polyphagy and primary host plants: oviposition preference versus larval performance in the lepidopteran pest Helicoverpa armigera. Arthropod-Plant Interactions, 1, 17-26.
71. Rasband, W.S. (2008) ImageJ. National Institutes of Health, Bethesda, Maryland. URL 1997-2011.
72. Reitz, S. & Adler, P. (1995) Fecundity and oviposition of Eucelatoria bryani, a gregarious parasitoid of Helicoverpa zea and Heliothis virescens. Entomologia Experimentalis et Applicata, 75, 175-181.
73. Reudler Talsma, J.H. (2007) Costs and benefits of iridoid glycosides in multitrophic systems. PhD thesis, Wageningen University, the Netherlands.
74. Sarfraz, M., Dosdall, L.M. & Keddie, B.A. (2009) Host plant nutritional quality affects the performance of the parasitoid Diadegma insulare. Biological Control, 51, 34-41.
75. ® Version 8.0.2. SAS Institute Inc., Cary, North Carolina.
76. Seidl, S.E. & King, B.H. (1993) Sex ratio response to host size in the parasitoid wasp Muscidifurax raptor. Evolution, 47, 1876-1882.
77. Singer, M.S., Rodrigues, D., Stireman, J.O. & Carriere, Y. (2004) Roles of food quality and enemy-free space in host use by a generalist insect herbivore. Ecology, 85, 2747-2753.
78. Slansky, F. & Scriber, J.M. (1985) Food consumption and utilization. Comprehensive Insect Physiology, Biochemistry and Pharmacology (ed. by G. A. Kerkut and L. I. Gilbert), pp. 87-163. Pergamon, Oxford, U.K.
79. Srygley, R.B., Lorch, P.D., Simpson, S.J. & Sword, G.A. (2009) Immediate protein dietary effects on movement and the generalised immunocompetence of migrating Mormon crickets Anabrus simplex (Orthoptera: Tettigoniidae). Ecological Entomology, 34, 663-668.
80. Stireman, J.O., O'Hara, J.E. & Wood, D.M. (2006) Tachinidae: Evolution, behavior, and ecology. Annual Review of Entomology, 51, 525-555.
81. Strand, M.R. & Pech, L.L. (1995) Immunological basis for compatibility in host-parasitoid relationships. Annual Review of Entomology, 40, 31-56.
82. Teder, T. & Tammaru, T. (2002) Cascading effects of variation in plant vigour on the relative performance of insect herbivores and their parasitoids. Ecological Entomology, 27, 94-104.
83. Tillman, P.G. & Cate, J.R. (1993) Effect of host size on adult size and sex ratio of Bracon mellitor (Hymenoptera: Braconidae). Biological Control, 22, 1161-1165.
84. Turlings, T.C.J., Tumlinson, J.H. & Lewis, W.J. (1990) Exploitation of herbivore-induced plant odors by herbivore-seeking parasitoid wasps. Science, 250, 1251-1253.
85. Ueno, T. (1998) Sex allocation by a parasitoid wasp (Hymenoptera: Ichneumonidae) to different host species: a question for the mechanism of host size estimation. Journal of Insect Behavior, 11, 811-821.
86. Vinson, S.B. (1990) How parasitoids deal with the immune system of their host: an overview. Archives of Insect Biochemistry and Physiology, 13, 3-27.
87. Visser, M.E. (1994) The importance of being large - the relationship between size and fitness in females of the parasitoid Aphaereta minuta (Hymenoptera: Braconidae). Journal of Animal Ecology, 63, 963-978.
88. Wagner, D.L. (2005) Caterpillars of Eastern North America. Princeton University Press, Princeton, New Jersey.
89. Wang, X.-Y., Yang, Z.-Q., Wu, H. & Gould, J.R. (2008) Effects of host size on the sex ratio, clutch size, and size of adult Spathius agrili, an ectoparasitoid of emerald ash borer. Biological Control, 44, 7-12.
90. Zalucki, M.P., Clarke, A.R. & Malcolm, S.B. (2002) Ecology and behavior of first instar larval Lepidoptera. Annual Review of Entomology, 47, 361-393.