Differential Performance of a Specialist and Two Generalist Herbivores and Their Parasitoids on Plantago lanceolata

Journal of Chemical Ecology

Volumn 37, Issue 7, 2011, Pages 765-778

  Reudler, Joanneke H ^a,b   Biere, Arjen ^a   Harvey, Jeff A ^a   van Nouhuys, Saskya ^c,d  

^a NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^b UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^c Department of Obstetrics Gynecology   (United States)

^d UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Chemical defense; Chrysodeixis chalcites; Cotesia marginiventris; Cotesia melitaearum; Hyposoter didymator; Immunocompromised host; Iridoid glycosides; Melitaea cinxia; Multitrophic interactions; Spodoptera exigua

Indexed keywords

AUCUBIN; CATALPOL; IRIDOID; PHEROMONE;

ADAPTATION; ALLELOCHEMICAL; BUTTERFLY; CHEMICAL DEFENSE; DICOTYLEDON; ENDOPARASITE; GENERALIST; HOST PLANT; IMMUNE RESPONSE; LARVA; LONGEVITY; MOTH; PARASITOID; PLANT DEFENSE; PLANT-HERBIVORE INTERACTION; PUPA; SPECIALIST; TRITROPHIC INTERACTION; WASP;

ADAPTATION; ANIMAL; ARMYWORM; ARTICLE; BUTTERFLY; CHEMISTRY; DRUG EFFECT; FEEDING BEHAVIOR; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; HYMENOPTERA; LARVA; PHYSIOLOGY; PLANT; PLANT LEAF; PLANTAGO;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BUTTERFLIES; FEEDING BEHAVIOR; HOST-PARASITE INTERACTIONS; HYMENOPTERA; IRIDOID GLUCOSIDES; LARVA; PHEROMONES; PLANT LEAVES; PLANTAGO; PLANTS, EDIBLE; SPODOPTERA;

CHRYSODEIXIS CHALCITES; COTESIA MARGINIVENTRIS; COTESIA MELITAEARUM; HYPOSOTER DIDYMATOR; MELITAEA CINXIA; PLANTAGO; PLANTAGO LANCEOLATA; SPODOPTERA EXIGUA;

EID: 79959655568     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-011-9983-7     Document Type: Article

References (95)

1. Adler, L. S., Schmitt, J., and Bowers, M. D. 1995. Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia 101: 75-85.
2. Agrawal, A. A. 2000. Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89: 493-500.
3. Ballabeni, P., Gotthard, K., Kayumba, A., and Rahier, M. 2003. Local adaptation and ecological genetics of host-plant specialization in a leaf beetle. Oikos 101: 70-78.
4. Bar, D., Gerlings, D., and Rossler, Y. 1979. Bionomics of the principal natural enemies attacking Heliothis armigera in cotton fields in Israel. Environ. Entomol. 8: 468-474.
5. Barbosa, P. 1988. Natural enemies and herbivore-plant interactions: influence of plant allelochemicals and host specificity, pp. 201-229, in P. Barbosa and D. K. Letourneau (eds.). Novel Aspects of Insect-Plant Interactions. John Wiley and Sons, New York.
6. Barbosa, P., Saunders, J. A., Kemper, J., Trumbule, R., Olechno, J., and Martinat, P. 1986. Plant allelochemicals and insect parasitoids. Effects of nicotine on Cotesia congregata (Say) (Hymenoptera, Braconidae) and Hyposoter annulipes (Cresson) (Hymenoptera, Ichneumonidae). J. Chem. Ecol. 12: 1319-1328.
7. Barbosa, P., Gross, P., and Kemper, J. 1991. Influence of plant allelochemicals on the tobacco hornworm and its parasitoid, Cotesia congregata. Ecology 72: 1567-1575.
8. Barton, K. E. 2007. Early ontogenetic patterns in chemical defense in Plantago (Plantaginaceae): genetic variation and trade-offs. Am. J. Bot. 94: 56-66.
9. Biere, A., Marak, H. B., and van Damme, J. M. M. 2004. Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs? Oecologia 140: 430-441.
10. Bowers, M. D. 1980. Unpalatability as a defense strategy of Euphydryas phaeton (Lepidoptera: Nymphalidae). Evolution 34: 586-600.
11. Bowers, M. D. 1981. Unpalatability as a defense strategy of western checkerspot butterflies (Euphydryas, Nymphalidae). Evolution 35: 367-375.
12. Bowers, M. D. 1984. Iridoid glycosides and host-plant specificity in larvae of the buckeye butterfly, Junonia coenia (Nymphalidae). J. Chem. Ecol. 10: 1567-1577.
13. Bowers, M. D. 1991. Iridoid glycosides, pp. 297-325, in G. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites. Academic Press, San Diego.
14. Bowers, M. D. 2003. Hostplant suitability and defensive chemistry of the Catalpa sphinx, Ceratomia catalpae. J. Chem. Ecol. 29: 2359-2367.
15. Bowers, M. D., and Collinge, S. K. 1992. Fate of iridoid glycosides in different life stages of the buckeye, Junonia coenia (Lepidoptera, Nymphalidae). J. Chem. Ecol. 18: 817-831.
16. Bowers, M. D., and Puttick, G. M. 1988. Response of generalist and specialist insects to qualitative allelochemical variation. J. Chem. Ecol. 14: 319-334.
17. Bowers, M. D., and Stamp, N. E. 1992. Chemical variation within and between individuals of Plantago lanceolata (Plantaginaceae). J. Chem. Ecol. 18: 985-995.
18. Bowers, M. D., Collinge, S. K., Gamble, S. E., and Schmitt, J. 1992. Effects of genotype, habitat, and seasonal variation on iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and the implications for insect herbivores. Oecologia 9: 201-207.
19. Camara, M. D. 1997a. Physiological mechanisms underlying the costs of chemical defence in Junonia coenia Hubner (Nymphalidae): a gravimetric and quantitative genetic analysis. Evol. Ecol. 11: 451-469.
20. Camara, M. D. 1997b. Predator responses to sequestered plant toxins in buckeye caterpillars: are tritrophic interactions locally variable? J. Chem. Ecol. 23: 2093-2106.
21. Campbell, B. C., and Duffey, S. S. 1979. Tomatine and parasitic wasps: potential incompatibility of plant antibiosis with biological control. Science 205: 700-702.
22. Clancy, K. M., and Price, P. W. 1987. Rapid herbivore growth enhances enemy attack: sublethal plant defenses remain a paradox. Ecology 68: 736-738.
23. Cooper, S. M., and Owen-Smith, N. 1986. Effects of plant senescence on large mammalian herbivores. Oecologia 68: 446-455.
24. Cornell, H. V., and Hawkins, B. A. 2003. Herbivore responses to plant secondary compounds: a test of phytochemical coevolution theory. Am. Nat. 161: 507-522.
25. Damtoft, S., Jensen, S. R., and Nielsen, B. J. 1983. The biosynthesis of iridoid glycosides from 8-epi-deoxyloganic acid. Biochemical Society Transactions 11: 593-594.
26. Darrow, K., and Bowers, M. D. 1997. Phenological and population variation in iridoid glycosides of Plantago lanceolata (Plantaginaceae). Biochem. Sys. Ecol. 25: 1-11.
27. Denno, R. F., and McClure, M. S. 1983. Variable Plants and Herbivores in Natural and Managed Systems. Academic Press, New York.
28. Duffey, S. S. 1980. Sequestration of plant natural products by insects. Annu. Rev. of Entomol. 25: 447-477.
29. Duffey, S. S., Bloem, K. A., and Campbell, B. C. 1986. Consequences of sequestration of plant natural products in plant-insect-parasitoid interactions, pp. 31-60, in D. J. Boethel and R. D. Eikenbary (eds.). Interactions of Plant Resistance and Parasitoids and Predators of Insects. Horwood, Chichester, UK.
30. Ehrlich, P. R., and Raven, P. H. 1964. Butterflies and plants: a study in coevolution. Evolution 18: 586-608.
31. Elzinga, J. A. 2002. The rearing of the gregarious koinobiont endoparasitoid Microplitis tristis (Hymenoptera: Braconidae) on its natural host Hadena bicruris (Lepidoptera: Noctuidae). Proc. Sect. Exp. Appl. Entomol. Netherl. Entomol. Soc. (NEV) 13: 109-115.
32. Fajer, E. D., Bowers, M. D., and Bazzaz, F. A. 1992. The effect of nutrients and enriched CO2 environments on production of carbon-based allelochemicals in Plantago: a test of the carbon/nutrient balance hypothesis. Am. Nat. 140: 707-723.
33. Figueiredo, E., Mexíca, A., Albajes, R., and Sekeroglu, E. 2000. Parasitoid complex associated with Lepidoptera on horticultural protected crops in the Oeste region of Portugal. IOBC WPRS Working Group "Integrated Control in Protected Crops, Mediterranean Climate". Bull. OILB SROP 23: 205-208.
34. Fraenkel, G. S. 1959. The raison d'étre of secondary plant substances. The odd chemicals arose as a means of protecting plants from insects and now guide insects to food. Science 129: 1466-1470.
35. Gauld, I. D., Gaston, K. J., and Janzen, D. H. 1992. Plant allelochemicals, tritrophic interactions and the anomalous diversity of tropical parasitoids-the nasty host hypothesis. Oikos 65: 353-357.
36. Godfray, H. C. J. 1994. Parasitoids: Behavioural and Evolutionary Ecology. Princeton University Press, Princeton, NJ.
37. Goodey, B. 1991. Chrysodeixis chalcites (Esper, 1789) (Lep.: Noctuidae): observations on the life cycle in captivity. Entomol. Rec. 103: 111-118.
38. Greischar, M. A., and Koskella, B. 2007. A synthesis of experimental work on parasite local adaptation. Ecol. Lett. 10: 418-434.
39. Gunasena, G. H., Vinson, S. B., and Williams, H. J. 1990. Effects of nicotine on growth, development, and survival of the tobacco budworm (Lepidoptera, Noctuidae) and the parasitoid Campoletis sonorensis (Hymenoptera, Ichneumonidae). J. Ecol. Entomol. 83: 1777-1782.
40. Harvey, J. A., and Strand, M. R. 2002. The developmental strategies of endoparasitoid wasps vary with host feeding ecology. Ecology 83: 2439-2451.
41. Harvey, J. A., Kadash, K., and Strand, M. R. 2000. Differences in larval feeding behavior correlate with altered developmental strategies in two parasitic wasps: implications for the size-fitness hypothesis. Oikos 88: 621-629.
42. Harvey, J. A., van Nouhuys, S., and Biere, A. 2005. Effects of quantitative variation in allelochemicals in Plantago lanceolata on development of a generalist and a specialist herbivore and their endoparasitoids. J. Chem. Ecol. 31: 287-302.
43. Harvey, J. A., Gols, R., Wagenaar, R., and Bezemer, T. M. 2007a. Development of an insect herbivore and its pupal parasitoid reflect differences in direct plant defense. J. Chem. Ecol. 33: 1556-1569.
44. Harvey, J. A., van Dam, N. M., Witjes, L. M. A., Soler, R., and Gols, R. 2007b. Effects of dietary nicotine on the development of an herbivore, its parasitoid and secondary hyperparasitoid over four trophic levels. Ecol. Entomol. 32: 15-23.
45. Ingram, W. R. 1981. The parasitoids of Spodoptera littoralis (Lep.: Noctuidae) and their role in population control in Cyprus. Entomophaga 26: 23-37.
46. Johnson, K. S. 1999. Comparative detoxification of plant (Magnolia virginiana) allelochemicals by generalist and specialist saturniid silkmoths. J. Chem. Ecol. 25: 253-269.
47. Kaltz, O., and Shykoff, J. A. 1998. Local adaptation in host-parasite systems. Heredity 81: 361-370.
48. Kankare, M., and Shaw, M. R. 2004. Molecular phylogeny of Cotesia (Hymenoptera: Braconidae: Microgastrinae) parasitoids associated with checkerspot butterflies. Mol. Phylogenet. Evol. 32: 207-220.
49. Kankare, M., van Nouhuys, S., and Hanski, I. 2005. Genetic divergence among host-specific cryptic species in Cotesia melitaearum aggregate (Hymenoptera: Braconidae), parasitoids of checkerspot butterflies. Ann. Entomol. Soc. Am. 98: 382-394.
50. Klingenberg, C. P., and Spence, J. R. 1997. On the role of body size for life-history evolution. Ecol. Entomol. 22: 55-68.
51. Kraaijeveld, A. R., and Godfray, H. C. J. 1997. Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389: 278-280.
52. Krombein, K. V., Hurd, P. D., Smith, D. R., and Burks, B. D. 1979. Catalogue of Hymenoptera of America North of Mexico. Smithsonian Institute Press, Washington D. C.
53. Kuussaari, M., van Nouhuys, S., Hellmann, J., and Singer, M. 2004. Larval biology of checkerspots, pp. 138-160, in P. R. EHRLICH and I. Haski, (eds.). On the Wings of Checkerspots: a Model System for Population Biology. University Press, Oxford.
54. Lampert, E. C., and Bowers, M. D. 2010. Host plant species affects the quality of the generalist Trichoplusia ni as a host for the polyembryonic parasitoid Copidosoma floridanum. Entomol. Exp. Appl. 134: 287-295.
55. Lampert, E. C., Zangerl, A. R., Berenbaum, M. R., and Ode, P. J. 2008. Tritrophic effects of xanthotoxin on the polyembryonic parasitoid Copidosoma sosares (Hymenoptera: Encyrtidae). J. Chem. Ecol. 34: 783-790.
56. Lampert, E. C., Dyer, L. A., and Bowers, M. D. 2010. Caterpillar chemical defense and parasitoid success: Cotesia congregata parasitism of Ceratomia catalpae. J. Chem. Ecol. 36: 992-998.
57. Laurentz, M. 2010. Diet quality can play critical role in the defence efficacy against parasitoids and pathogens in Glanville fritillary (Melitaea cinxia). Master Thesis. University of Jyväskylä.
58. Leather, S. R. 1988. Size, reproductive potential and fecundity in insects: things aren't as simple as they seem. Oikos 51: 386-389.
59. Lei, G. C., Vikberg, V., Nieminen, M., and Kuussaari, M. 1997. The parasitoid complex attacking Finnish populations of the Glanville fritillary Melitaea cinxia (Lep: Nymphalidae), an endangered butterfly. J. Nat. Hist. 31: 635-648.
60. Li, X. C., Baudry, J., Berenbaum, M. R., and Schuler, M. A. 2004. Structural and functional divergence of insect CYP6B proteins: from specialist to generalist cytochrome P450. Proc. Natl. Acad. Sci. U. S. A. 101: 2939-2944.
61. Macel, M., Klinkhamer, P. G. L., Vrieling, K., and van Der Meijden, E. 2002. Diversity of pyrrolizidine alkaloids in Senecio species does not affect the specialist herbivore Tyria jacobaeae. Oecologia 133: 541-550.
62. Macel, M., Bruinsma, M., Dijkstra, S. M., Ooijendijk, T., Niemeyer, H. M., and Klinkhamer, P. G. L. 2005. Differences in effects of pyrrolizidine alkaloids on five generalist insect herbivore species. J. Chem. Ecol. 31: 1493-1508.
63. Mallampalli, N., Barbosa, P., and Weinges, K. 1996. Effects of condensed tannins and catalpol on growth and development of Compsilura concinnata (Diptera: Tachinidae) reared in gypsy moth (Lepidoptera: Lymantriidae). J. Entomol. Sci. 31: 289-300.
64. Marak, H. B., Biere, A., and van Damme, J. M. M. 2000. Direct and correlated responses to selection on iridoid glycosides in Plantago lanceolata L. J. Evol. Biol. 13: 985-996.
65. Marak, H. B., Biere, A., and van Damme, J. M. M. 2003. Fitness costs of chemical defense in Plantago lanceolata L.: Effects of nutrient and competition stress. Evolution 57: 2519-2530.
66. Nappi, A. J. 1975. Parasite encapsulation in insects, pp. 293-356, in K. Maramoch and R. Shope, (eds.). Invertebrate Immunity. Academic Press, New York.
67. Nieminen, M., Suomi, J., van Nouhuys, S., Sauri, P., and Riekkola, M. L. 2003. Effect of iridoid glycoside content on oviposition host plant choice and parasitism in a specialist herbivore. J. Chem. Ecol. 29: 823-844.
68. Nishida, R. 2002. Sequestration of defensive substances from plants by Lepidoptera. Annu. Rev. Entomol. 47: 57-92.
69. Ode, P. J., 2006. Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu. Rev. Entomol. 51: 163-185.
70. Ojala, K., Julkunen-Titto, R., Lindstrom, L., and Mappes, J. 2005. Diet affects the immune defence and life-history traits of an Arctiid moth Parasemia plantaginis. Evol. Ecol. Res. 7: 1153-1170.
71. Paradise, C. J., and Stamp, N. E. 1993. Episodes of unpalatable prey reduce consumption and growth of juvenile praying mantids. J. Insect Behav. 6: 155-166.
72. Pereyra, P. C., and Bowers, M. D. 1988. Iridoid glycosides as oviposition stimulants for the buckeye butterfly, Junonia coenia (Nymphalidae). J. Chem. Ecol. 14: 917-928.
73. Puttick, G. M., and Bowers, M. D. 1988. Effect of qualitative and quantitative variation in allelochemicals on generalist insects: iridoid glycosides and the southern army worm. J. Chem. Ecol. 14: 335-351.
74. Quicke, D. L. J. 1997. Parasitic wasps. Chapman and Hall, London.
75. Renwick, J. A. A., Zhang, W. Q., Haribal, M., Attygalle, A. B., and Lopez, K. D. 2001. Dual chemical barriers protect a plant against different larval stage of an insect. J. Chem. Ecol. 27: 1575-1583.
76. Reudler Talsma J. H. 2007. Costs and benefits or iridoid glycosides in multitrophic systems. Ph. D. dissertation. Wageningen University.
77. Reudler Talsma, J. H., Elzinga, J. A., Harvey, J. A., and Biere, A. 2007. Optimum and maximum host size at parasitism for the endoparasitoid Hyposoter didymator (Hymenoptera: Ichneumonidae) differ greatly between two host species. Environ. Entomol. 36: 1048-1053.
78. Reudler Talsma, J. H., Biere A., Harvey, J. A., and van Nouhuys, S. 2008. Oviposition cues for a specialist butterfly: plant chemistry and size. J. Chem. Ecol. 34: 1202-1212.
79. Rhoades, D. F. 1979. Evolution of plant chemical defense against herbivores. pp. 3-54, in Rosenthal G. A., and Janzen D. H. (eds.) Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, New York.
80. Saastamoinen, M. 2007. Life-history, genotypic, and environmental correlates of clutch size in the Glanville fritillary butterfly. Ecol. Entomol. 32: 235-242.
81. Saastamoinen, M., van Nouhuys, S., Nieminen, M., O'Hara, B., and Suomi, J. 2007. Development and survival of a specialist herbivore, Melitaea cinxia, on host plants producing high and low concentrations of iridoid glycosides. Ann. Zool. Fenn. 44: 70-80.
82. Sagar, G. R., and Harper, J. L. 1964. Biological flora of the British isles. Plantago major L., Plantago media L. and Plantago lanceolata L. J. Ecol. 52: 189-221.
83. Schneider, M. I., Smagghe, G., Gobbi, A., and Viñuela, E. 2003. Toxicity and pharmacokinetics of insect growth regulators and other novel insecticides on pupae of Hyposoter didymator (Hymenoptera: Ichneumonidae), a parasitoid of early larval instars of Lepidopteran pests. J. Ecol. Entomol. 4: 1054-1065.
84. Singer, M. S. 2008. Evolutionary Ecology of Polyphagy. pp. 29-42, in Tilmon, K. J. (Ed.) Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects. University of California Press, Berkeley, CA.
85. Smilanich, A. M., Dyer, L. A., Chambers, J. Q., and Bowers, M. D. 2009. Immunological cost of chemical defence and the evolution of herbivore diet breath. Ecol. Lett. 12: 612-621.
86. Suomi, J., Sirén, H., Weidmer, S. K., and Riekkola, M. 2001. Isolation of aucubin and catalpol from Melitaea cinxia larvae and quantification by micellar electrokinetic capillary chromatography. Anal. Chim. Acta 429: 91-99.
87. Suomi, J., Sirén, H., Jussila, M., Wiedner, S. K., and Riekkola, M. L. 2003. Determination of iridoid glycosides in larvae and adults of butterfly Melitaea cinxia by partial filling micellar electrokinetic capillary chromatography-electrospray ionisation mass spectrometry. Anal. Bioanal. Chem. 376: 884-889.
88. Sznajder, B., and Harvey, J. A. 2003. Second and third trophic level effects of differences in plant species reflect dietary specialisation of herbivores and their endoparasitoids. Entomol. Exp. Appl. 109: 73-82.
89. Tingle, F. C., and Mitchell, E. R. 1977. Seasonal populations of armyworms and loopers at Hastings, Florida. Fla. Entomol. 60: 115-122.
90. van Nouhuys, S., and Punju, E. 2010. Coexistence of competing parasitoids: which is the fugitive and where does it hide? Oikos 119: 61-70.
91. van Nouhuys, S., Singer, M. C., and Nieminen, M. 2003. Spatial and temporal patterns of caterpillar performance and the suitability of two host plant species. Ecol. Entomol. 28: 193-202.
92. Vinson, S. B. 1990. Physiological interactions between the host genus Heliothis and its guild of parasitoids. Arch. Insect Biochem. 13: 63-81.
93. Wilson, J. W. 1934. The asparagus caterpillar: its life history and control. Fla. Agr. Exp. Sta. Bull. 271: 1-26.
94. Wu, L., and Antonovics, J. 1975. Experimental ecological genetics in Plantago. I. Induction of roots and shoots on leaves for large scale vegetative propagation and metal tolerance testing in P. lanceolata. New Phytol. 75: 277-282.
95. Zovi, D., Stastny, M., Battisti, A., and Larsson, S. 2008. Ecological costs on local adaptation of an insect herbivore imposed by host plants and enemies. Ecology 89: 1388-1398.