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Pathogen resistance in the moth Orgyia antiqua: direct influence of host plant dominates over the effects of individual condition

Published online by Cambridge University Press:  14 July 2010

S.-L. Sandre ,
T. Tammaru  and
H.M.T. Hokkanen
S.-L. Sandre*
Affiliation:
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014, Tartu, Estonia
T. Tammaru
Affiliation:
Department of Zoology, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51014, Tartu, Estonia
H.M.T. Hokkanen
Affiliation:
Department of Applied Biology, University of Helsinki, Finland
*
*Author for correspondence Fax: +372 7375 830 E-mail: siiri-lii.sandre@ut.ee
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Abstract

The role of pathogens in insect ecology is widely appreciated but remains insufficiently explored. Specifically, there is little understanding about the sources of the variation in the outcome of insect-pathogen interactions. This study addresses the extent to which immune traits of larvae and pupae of the moth Orgyia antiqua L. (Lepidoptera: Lymantriidae) depend on the host plant species and individual condition of the insects. The two host plants, Salix myrsinifolia Salisb. and S. viminalis L., were chosen because they differ in the concentration of phenolic glycosides, harmful to most polyphagous insects. Individual condition was assumed to be reflected in body weight and development time, and was manipulated by rearing larvae either singly or in groups of four. The resistance traits recorded were survival and time to death after fungal infection in the larval stage and the efficiency of encapsulating a nylon implant by the pupae. The survival of the infected larvae was mainly determined by the species of the host plant. Encapsulation response was not associated with the resistance to the pathogen, suggesting that the host plant affected the pathogen rather than the immune system of the insect. Interestingly, the host plant supporting better larval growth led to inferior resistance to the pathogen, indicating a trade-off between different aspects of host plant quality.

Keywords

tritrophic interactiondensity dependent prophylaxisMetarhizium anisopliaepathogen resistancehost plant quality
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 101 , Issue 1 , February 2011 , pp. 107 - 114
Copyright
Copyright © Cambridge University Press 2010

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References

Applebaum, S.W. & Heifetz, Y. (1999) Density-dependent physiological phase in insects. Annual Review of Entomology 44, 317–341.CrossRefGoogle ScholarPubMed
Blanckenhorn, W.U. (2000) The evolution of body size: What keeps organisms small? Quarterly Review of Biology 75, 385–407.Google Scholar
Boucias, D.G. & Pendland, J.C. (1998) Principles of Insect Pathology. 1st ed. Dordrecht, The Netherlands, Kluwer Academic Publishers.Google Scholar
Cory, J.S. & Hoover, K. (2006) Plant-mediated effects in insect-pathogen interactions. Trends in Ecology & Evolution 21, 278–286.CrossRefGoogle ScholarPubMed
Cotter, S.C. & Wilson, K. (2002) Heritability of immune function in the caterpillar Spodoptera littoralis. Heredity 88, 229–234.CrossRefGoogle ScholarPubMed
Cotter, S.C., Hails, R.S., Cory, J.S. & Wilson, K. (2004) Density-dependent prophylaxis and condition-dependent immune function in Lepidopteran larvae: a multivariate approach. Journal of Animal Ecology 73, 283–293.CrossRefGoogle Scholar
Dwyer, G., Elkinton, J.S. & Buonaccorsi, J.P. (1997) Host heterogeneity in susceptibility and disease dynamics: Tests of a mathematical model. The American Naturalist 150, 685–707.CrossRefGoogle ScholarPubMed
Esperk, T. & Tammaru, T. (2006) Determination of female-biased sexual size dimorphism in moths with a variable instar number: The role of additional instars. European Journal of Entomology 103, 575–586.Google Scholar
Fox, C.W., Roff, D.A. & Fairbairn, D.J. (2001) Evolutionary Ecology: Concepts and Case Studies. Oxford, UK, Oxford University Press.Google Scholar
Freitak, D., Ots, I., Vanatoa, A. & Hõrak, P. (2003) Immune response is energetically costly in white cabbage butterfly pupae. Proceedings of the Royal Society of London, Series B: Biological Sciences 270, S220–S222.CrossRefGoogle ScholarPubMed
Goulson, D. & Cory, J.S. (1995) Responses of Mamestra brassicae (Lepidoptera, Noctuidae) to crowding – interactions with disease resistance, colour phase and growth. Oecologia 104, 416–423.CrossRefGoogle ScholarPubMed
Gunn, A. (1998) The determination of larval phase coloration in the African armyworm, Spodoptera exempta and its consequences for thermoregulation and protection from UV light. Entomologia Experimentalis et Applicata 86, 125–133.Google Scholar
Hare, J.A. & Andreadis, T.G. (1983) Variation in the susceptibility of Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) when reared on different host plants to the fungal pathogen, Beauveria bassiana in the field and laboratory. Environmental Entomology 12, 1892–1897.CrossRefGoogle Scholar
Honek, A. (1993) Intraspecific variation in body size and fecundity in insects – a general relationship. Oikos 66, 483–492.CrossRefGoogle Scholar
Hoover, K., Washburn, J.O. & Volkman, L.E. (2000) Midgut-based resistance of Heliothis virescens to baculovirus infection mediated by phytochemicals in cotton. Journal of Insect Physiology 46, 999–1007.CrossRefGoogle ScholarPubMed
Hõrak, P., Ots, I., Vellau, H., Spottiswoode, C. & Moller, A.P. (2001) Carotenoid-based plumage colouration reflects hemoparasite infection and local survival in breeding great tits. Oecologia 126, 166–173.Google Scholar
Julkunen-Tiitto, R. (1986) A chemotaxonomic survey of phenolic glycosides in leaves of northern Salicaceae species. Phytochemistry 25, 663–667.Google Scholar
Kapari, L., Haukioja, E., Rantala, M.J. & Ruuhola, T. (2006) Defoliating insect immune defence interacts with induced plant defence during a population outbreak. Ecology 87, 291–296.CrossRefGoogle ScholarPubMed
Kepler, R.M. & Bruck, D.J. (2006) Examination of the interaction between the black vine weevil (Coleoptera: Curculionidae) and an entomopathogenic fungus reveals a new tritrophic interaction. Environmental Entomology 35, 1021–1029.CrossRefGoogle Scholar
Klemola, N., Klemola, T., Rantala, M.J. & Ruuhola, T. (2007) Natural host-plant quality affects immune defence of an insect herbivore. Entomologia Experimentalis et Applicata 123, 167–176.Google Scholar
Klingen, I., Hajek, A., Meadow, R. & Renwick, J.A.A. (2002) Effect of brassicaceous plants on the survival and infectivity of insect pathogenic fungi. Biocontrol 47, 411–425.Google Scholar
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.CrossRefGoogle Scholar
Lindroth, R.L., Scriber, J.M. & Hsia, M.T.S. (1988) Chemical Ecology of the Tiger Swallowtail: Mediation of Host Use by Phenolic Glycosides. Ecology 69, 814–822.Google Scholar
Lindroth, R.L., Roth, S., Kruger, E.L., Volin, J.C. & Koss, P.A. (1997) CO2-mediated changes in aspen chemistry: Effects on gypsy moth performance and susceptibility to virus. Global Change Biology 3, 279–289.Google Scholar
McVean, R.I.K., Sait, S.M., Thompson, D.J. & Begon, M. (2002) Dietary stress reduces the susceptibility of Plodia interpunctella to infection by a granulovirus. Biological Control 25, 81–84.CrossRefGoogle Scholar
Mowlds, P., Barron, A. & Kavanagh, K. (2008) Physical stress primes the immune response of Galleria mellonella larvae to infection by Candida albicans. Microbes and Infection 10, 628–634.CrossRefGoogle ScholarPubMed
Navon, A., Hare, J.D. & Federici, B.A. (1993) Interactions among Heliothis virescens larvae, cotton condensed tannin and the CryIA(c) delta-entotoxin of Bacillus thuringensis. Journal of Chemical Ecology 19, 2485–2499.Google Scholar
Ojala, K., Julkunen-Tiitto, R., Lindström, 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.Google Scholar
Ots, I., Freitak, D. & Vanatoa, A. (2005) Expression of immunity and general condition in the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae), in relation to origin and gender. Entomological Science 8, 173–178.CrossRefGoogle Scholar
Plymale, R., Grove, M.J., Cox-Foster, D., Ostiguy, N. & Hoover, K. (2008) Plant-mediated alteration of the peritrophic matrix and baculovirus infection in lepidopteran larvae. Journal of Insect Physiology 54, 737–749.CrossRefGoogle ScholarPubMed
Rantala, M.J. & Roff, D.A. (2005) An analysis of trade-offs in immune function, body size and development time in the Mediterranean Field Cricket, Gryllus bimaculatus. Functional Ecology 19, 323–330.Google Scholar
Rantala, M.J., Koskimäki, J., Taskinen, J., Tynkkynen, K. & Suhonen, J. (2000) Immunocompetence, developmental stability and wingspot size in the damselfly Calopteryx splendens L. Proceedings of the Royal Society of London, Series B 267, 2453–2457.CrossRefGoogle ScholarPubMed
Raymond, B., Vanbergen, A., Pearce, I., Hartley, S.E., Cory, J.S. & Hails, R.S. (2002) Host plant species can influence the fitness of herbivore pathogens: the winter moth and its nucleopolyhedrovirus. Oecologia 131, 533–541.Google Scholar
Reitz, S.R. & Trumble, J.T. (1997) Effects of linear furanocoumarins on the herbivore Spodoptera exigua and the parasitoid Archytas marmoratus: host quality and parasitoid success. Entomologia Experimentalis et Applicata 84, 9–16.CrossRefGoogle Scholar
Rolff, J. (2001) Effects of age and gender on immune function of dragonflies (Odonata, Lestidae) from a wild population. Canadian Journal of Zoology 79, 2176–2180.Google Scholar
Saks, L., Ots, I. & Hõrak, P. (2003) Carotenoid-based plumage colouration of male greenfinches reflects health and immunocompetence. Oecologia 134, 301–307.CrossRefGoogle ScholarPubMed
Sanders, A.E., Scarborough, C., Layen, S.J., Kraaijeveld, A.R. & Godfray, H.C. (2005) Evolutionary change in parasitoid resistance under crowded conditions in Drosophila melanogaster. Evolution 59, 1292–1299.Google ScholarPubMed
Sandre, S.-L., Tammaru, T., Esperk, T., Julkunen-Tiitto, R. & Mappes, J. (2007) Carotenoid-based colour polyphenism in a moth species: search for fitness correlates. Entomologia Experimentalis et Applicata 124, 269–277.CrossRefGoogle Scholar
Schmid-Hempel, P. & Ebert, D. (2003) On the evolutionary ecology of specific immune defence. Trends in Ecology & Evolution 18, 27–32.Google Scholar
Schoonhoven, L.M., van Loon, J.J.A. & Dicke, M. (2005) Insect-Plant Biology. 2nd edn. New York, Oxford University Press.Google Scholar
Schwarzenbach, G.A. & Ward, P.I. (2006) Responses to selection on phenoloxidase activity in yellow dung flies. Evolution 60, 1612–1621.Google Scholar
Singer, M.S., Carriere, Y., Theuring, C. & Hartmann, T. (2004a) Disentangling Food Quality from Resistance against Parasitoids: Diet Choice by a Generalist Caterpillar. The American Naturalist 164, 424–429.CrossRefGoogle ScholarPubMed
Singer, M.S., Rodrigues, D., Stireman, J.O. & Carriere, Y. (2004b) Roles of food quality and enemy-free space in host use by a generalist insect herbivore. Ecology 85, 2747–2753.CrossRefGoogle Scholar
Tammaru, T., Ruohomäki, K. & Montola, M. (2000) Crowding-induced plasticity in Epirrita autumnata (Lepidoptera: Geometridae): weak evidence of specific modifications in reaction norms. Oikos 90, 171–181.CrossRefGoogle Scholar
Tammaru, T., Esperk, T. & Castellanos, I. (2002) No evidence for costs of being large in females of Orgyia spp. (Lepidoptera, Lymantriidae): larger is always better. Oecologia 133, 430–438.Google Scholar
Turchin, P., Wood, S.N., Ellner, S.P., Kendall, B.E., Murdoch, W.W., Fischlin, A., Casas, J., McCauley, E. & Briggs, C.J. (2003) Dynamical effects of plant quality and parasitism on population cycles of larch budmoth. Ecology 84, 1207–1214.Google Scholar
Ugine, T.A., Wraight, S.P. & Sanderson, J.P. (2007) A tritrophic effect of host plant on susceptibility of western flower thrips to the entomopathogenic fungus Beauveria bassiana. Journal of Invertebrate Pathology 96, 162–172.Google Scholar
Vänninen, I., Hokkanen, H. & Tyni-Juslin, J. (1999) Screening of field performance of entomopathogenic fungi and nematodes against cabbage root flies (Delia radicum L. and D. floralis (Fall.), Diptera, Anthomyiidae). Acta Agriculturae Scandinavica Section B-Soil and Plant Science 49, 167–183.Google Scholar
Vega, F.E., Dowd, P.F., McGuire, M.R., Jackson, M.A. & Nelsen, T.C. (1997) In Vitro Effects of Secondary Plant Compounds on Germination of Blastospores of the Entomopathogenic Fungus Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes). Journal of Invertebrate Pathology 70, 209–213.Google Scholar
Vestergaard, S., Cherry, A., Keller, S. & Goettel, M. (2003) Safety of hyphomycete fungi as microbial control agents. pp. 35–62 in Hokkanen, H.M.T. & Hajek, A.E. (Eds) Environmental Impacts of Microbial Insecticides. Dordrecht, Kluwer Academic Publishers.Google Scholar
Villalon, J.M., Ghosh, A. & Jacobs-Lorena, M. (2003) The peritrophic matrix limits the rate of digestion in adult Anopheles stephensi and Aedes aegypti mosquitoes. Journal of Insect Physiology 49, 891–895.Google Scholar
Vilmos, P. & Kurucz, E. (1998) Insect immunity: evolutionary roots of the mammalian innate immune system. Immunology Letters 62, 59–66.CrossRefGoogle ScholarPubMed
Wilson, K. & Cotter, S.C. (2009) Density-dependent prophylaxis in insects. pp 191–231 in Whitman, D.W. & Ananthakrishnan, T.N. (Eds) Phenotypic Plasticity of Insects: Mechanisms and Consequences. Enfield, NH, USA, Science Publishers.Google Scholar
Wilson, K., Cotter, S.C., Reeson, A.F. & Pell, J.K. (2001) Melanism and disease resistance in insects. Ecology Letters 4, 637–649.Google Scholar
Wilson, K., Thomas, M.B., Blanford, S., Doggett, M., Simpson, S.J. & Moore, S.L. (2002) Coping with crowds: Density-dependent disease resistance in desert locusts. Proceedings of the National Academy of Sciences 99, 5471–5475.CrossRefGoogle ScholarPubMed
Wilson, K., Knell, R., Boots, M. & Koch-Osborne, J. (2003) Group living and investment in immune defence: an interspecific analysis. Journal of Animal Ecology 72, 133–143.Google Scholar
Yang, S., Ruuhola, T., Haviola, S. & Rantala, M.J. (2008) Effects of host-plant shift on immune and other key life-history traits of an eruptive Geometrid, Epirrita autumnata (Borkhausen). Ecological Entomology 33, 510–516.Google Scholar
Yourth, C.P., Forbes, M.R. & Baker, R.L. (2002) Sex differences in melanotic encapsulation responses (immunocompetence) in the damselfly Lestes forcipatus Rambur. Canadian Journal of Zoology 80, 1578–1583.Google Scholar
Zuk, M. & Stoehr, A.M. (2002) Immune defence and host life history. The American Naturalist 160, S9–S22.Google Scholar