Skip to main content Accessibility help
×
Home

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

  • S.-L. Sandre (a1), T. Tammaru (a1) and H.M.T. Hokkanen (a2)

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.

Copyright

Corresponding author

*Author for correspondence Fax: +372 7375 830 E-mail: siiri-lii.sandre@ut.ee

References

Hide All
Applebaum, S.W. & Heifetz, Y. (1999) Density-dependent physiological phase in insects. Annual Review of Entomology 44, 317341.
Blanckenhorn, W.U. (2000) The evolution of body size: What keeps organisms small? Quarterly Review of Biology 75, 385407.
Boucias, D.G. & Pendland, J.C. (1998) Principles of Insect Pathology. 1st ed. Dordrecht, The Netherlands, Kluwer Academic Publishers.
Cory, J.S. & Hoover, K. (2006) Plant-mediated effects in insect-pathogen interactions. Trends in Ecology & Evolution 21, 278286.
Cotter, S.C. & Wilson, K. (2002) Heritability of immune function in the caterpillar Spodoptera littoralis. Heredity 88, 229234.
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, 283293.
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, 685707.
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, 575586.
Fox, C.W., Roff, D.A. & Fairbairn, D.J. (2001) Evolutionary Ecology: Concepts and Case Studies. Oxford, UK, Oxford University Press.
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, S220S222.
Goulson, D. & Cory, J.S. (1995) Responses of Mamestra brassicae (Lepidoptera, Noctuidae) to crowding – interactions with disease resistance, colour phase and growth. Oecologia 104, 416423.
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, 125133.
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, 18921897.
Honek, A. (1993) Intraspecific variation in body size and fecundity in insects – a general relationship. Oikos 66, 483492.
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.
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, 166173.
Julkunen-Tiitto, R. (1986) A chemotaxonomic survey of phenolic glycosides in leaves of northern Salicaceae species. Phytochemistry 25, 663667.
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, 291296.
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, 10211029.
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, 167176.
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, 411425.
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, 287295.
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, 814822.
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, 279289.
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, 8184.
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, 628634.
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, 24852499.
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, 11531170.
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, 173178.
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, 737749.
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, 323330.
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, 24532457.
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, 533541.
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.
Rolff, J. (2001) Effects of age and gender on immune function of dragonflies (Odonata, Lestidae) from a wild population. Canadian Journal of Zoology 79, 21762180.
Saks, L., Ots, I. & Hõrak, P. (2003) Carotenoid-based plumage colouration of male greenfinches reflects health and immunocompetence. Oecologia 134, 301307.
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, 12921299.
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, 269277.
Schmid-Hempel, P. & Ebert, D. (2003) On the evolutionary ecology of specific immune defence. Trends in Ecology & Evolution 18, 2732.
Schoonhoven, L.M., van Loon, J.J.A. & Dicke, M. (2005) Insect-Plant Biology. 2nd edn. New York, Oxford University Press.
Schwarzenbach, G.A. & Ward, P.I. (2006) Responses to selection on phenoloxidase activity in yellow dung flies. Evolution 60, 16121621.
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, 424429.
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, 27472753.
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, 171181.
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, 430438.
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, 12071214.
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, 162172.
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, 167183.
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, 209213.
Vestergaard, S., Cherry, A., Keller, S. & Goettel, M. (2003) Safety of hyphomycete fungi as microbial control agents. pp. 3562 in Hokkanen, H.M.T. & Hajek, A.E. (Eds) Environmental Impacts of Microbial Insecticides. Dordrecht, Kluwer Academic Publishers.
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, 891895.
Vilmos, P. & Kurucz, E. (1998) Insect immunity: evolutionary roots of the mammalian innate immune system. Immunology Letters 62, 5966.
Wilson, K. & Cotter, S.C. (2009) Density-dependent prophylaxis in insects. pp 191231 in Whitman, D.W. & Ananthakrishnan, T.N. (Eds) Phenotypic Plasticity of Insects: Mechanisms and Consequences. Enfield, NH, USA, Science Publishers.
Wilson, K., Cotter, S.C., Reeson, A.F. & Pell, J.K. (2001) Melanism and disease resistance in insects. Ecology Letters 4, 637649.
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, 54715475.
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, 133143.
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, 510516.
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, 15781583.
Zuk, M. & Stoehr, A.M. (2002) Immune defence and host life history. The American Naturalist 160, S9–S22.

Keywords

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

  • S.-L. Sandre (a1), T. Tammaru (a1) and H.M.T. Hokkanen (a2)

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed