Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-25T06:40:48.270Z Has data issue: false hasContentIssue false

Larval diet prior to and following virus ingestion influences the efficacy of two nucleopolyhedroviruses in whitemarked tussock moth (Orgyia leucostigma) caterpillars

Published online by Cambridge University Press:  28 May 2012

Garrett Brodersen*
Affiliation:
Faculty of Forestry and Environmental Management, University of New Brunswick, Fredericton, New Brunswick, Canada E3B 6C2
Rob Johns
Affiliation:
Natural Resources Canada, Canadian Forest Service – Atlantic Forestry Centre, PO Box 4000, 1350 Regent Street, Fredericton, New Brunswick, Canada E3B 5P7
Renée Lapointe
Affiliation:
Sylvar Technologies Inc., 1350 Regent Street, Fredericton, New Brunswick, Canada E3B 5P7
David Thumbi
Affiliation:
Sylvar Technologies Inc., 1350 Regent Street, Fredericton, New Brunswick, Canada E3B 5P7
Graham Thurston
Affiliation:
Natural Resources Canada, Canadian Forest Service – Atlantic Forestry Centre, PO Box 4000, 1350 Regent Street, Fredericton, New Brunswick, Canada E3B 5P7
Christopher J. Lucarotti
Affiliation:
Natural Resources Canada, Canadian Forest Service – Atlantic Forestry Centre, PO Box 4000, 1350 Regent Street, Fredericton, New Brunswick, Canada E3B 5P7
Dan Quiring
Affiliation:
Faculty of Forestry and Environmental Management, University of New Brunswick, Fredericton, New Brunswick, Canada E3B 6C2
*
1Corresponding author (e-mail: gdbrodersen@gmail.com).

Abstract

Food quality can influence the performance of immature insects and their interactions with pathogens, such as viruses. In manipulative field studies, virus-free caterpillars of the whitemarked tussock moth (WMTM) (Orgyia leucostigma (Smith)) had higher survival, more female-biased sex ratios, and were larger when feeding on white birch (Betula papyrifera Marshall) versus balsam fir (Abies balsamea (Linnaeus) Miller) or red spruce (Picea rubens Sargent). Subsequent laboratory studies with two nucleopolyhedroviruses, derived from WMTMs and Douglas-fir tussock moths, indicated that caterpillars fed high quality food (i.e., artificial diet) prior to infection had less mortality associated with virus infection than those feeding on lower quality foliage (i.e., birch). In field studies, caterpillars fed birch following infection had significantly lower mortality than those feeding on relatively lower quality foliage (i.e., balsam fir). We postulate that higher nutritional quality in artificial diet relative to birch (previrus-ingestion nutrition) and in birch relative to balsam fir foliage (postvirus-ingestion nutrition) has a positive effect on the ability of tussock moth caterpillars to resist or recover from viral infections, although the specific mechanisms responsible for observed resistance remain unclear.

Résumé

La qualité des éléments nutritifs peut influencer la performance des insectes immatures ainsi que leurs interactions avec leurs pathogènes, tels que les virus. Des études de terrains indiquent que les chenilles à houppes blanches (Orgyia leucostigma (Smith)) ont une meilleure survie, une proportion des sexes biaisée vers les femelles et sont plus grosses quand elles se nourrissent de bouleau à papier (Betula papyrifera Marshall) plutôt que de sapin baumier (Abies balsamea (Linnaeus) Miller) ou d’épinette rouge (Picea rubens Sargent). Des études de laboratoire ont ensuite indiqué que les chenilles nourries d'une diète de haute qualité (par ex., diète artificielle) avant l'ingestion virale avaient un taux de mortalité associé à deux nucléopolyhedrovirus isolés de la chenille à houppes blanches et de la chenille à houppes du Douglas taxifolié moins élevé que celles nourries de feuillage de moindre qualité (c.-à-d., bouleau). Des études de terrain ont aussi démontré que la mortalité de chenilles nourries de bouleau après l'infection était significativement moindre que celle des chenilles nourries de feuillage d'une qualité comparativement moindre (c.-à-d., sapin baumier). Nous postulons que la qualité nutritionnelle supérieure de la diète artificielle comparativement au bouleau (nutrition pré-ingestion virale), et du bouleau comparativement au sapin baumier (nutrition postingestion virale) a eu un effet positif sur la capacité des chenilles à houppes blanche à parer ou à récupérer des infections virales; cependant les mécanismes spécifiques qui sont responsables de cette résistance demeurent incertains.

Type
Original Article
Copyright
Copyright © Entomological Society of Canada 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abell, D.H.Gilbert, F.F. 1974. Nutrient content of fertilized deer browse in Maine. Journal of Wildlife Management, 38: 517524.CrossRefGoogle Scholar
Anderson, R.M.May, R.M. 1980. Infectious diseases and population cycles of forest insects. Science, 210: 658661.CrossRefGoogle ScholarPubMed
Awmack, C.S.Leather, S.R. 2002. Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology, 47: 817844.CrossRefGoogle ScholarPubMed
Barbehenn, R.V.Martin, M.M. 1992. The protective role of the peritrophic membrane in the tannin-tolerant larvae of Orgyia leucostigma (Lepidoptera). Journal of Insect Physiology, 38: 973980.CrossRefGoogle Scholar
Bell, R.A., Owens, D.C., Shapiro, M., Tardif, J.R. 1981. Development of mass rearing technology. In The gypsy moth: research toward integrated pest management. Vol. 1584. Edited by C.C. Doane and M.L. McManus. Technical Bulletin. United States Department of Agriculture Forest Service, Washington, DC, pp. 599633.Google Scholar
Bernays, E.A. 1978. Tannins: an alternative view point. Entomologia Experimentalis et Applicata, 24: 4453.CrossRefGoogle Scholar
Bernays, E.A.Minkenburg, O.P.J.M. 1997. Insect herbivores: different reasons for being a generalist. Ecology, 78: 11571169.CrossRefGoogle Scholar
Carisey, N.Bauce, E. 1997. Balsam fir foliar chemistry in middle and lower crowns and spruce budworm growth, development, food and nitrogen utilization. Journal of Chemical Ecology, 23: 19631978.CrossRefGoogle Scholar
Cunningham, J.C.Kaupp, W.J. 1995. Insect viruses. In Forest pests in Canada. Edited by J.A. Armstrong and W.G.H. Ives. Natural Resources Canada, Science and Sustainable Development Directorate, Ottawa. pp. 327340.Google Scholar
Embree, D.G., Elgee, D.E., Estabrooks, G.F. 1984. Orgyia leucostigma (J. E. Smith), whitemarked tussock moth (Lepidoptera: Lymantriidae). In Biological control programmes against insects and weeds in Canada 1969–1980. Edited by J.S. Keller and M.A. Hulme. Commonwealth Agricultural Bureaux, Slough, England. pp. 359361.Google Scholar
Engelhard, E.K., Kam-Morgan, L.N.W., Washburn, J.O., Volkman, L.E. 1994. The insect tracheal system: a conduit for the systemic spread of Autographa californica M nuclear polyhedrosis virus. Proceedings of the National Academy of Science of the United States of America, 91: 32243227.CrossRefGoogle ScholarPubMed
Erlandson, M.E. 2008. Insect pest control by viruses. In Encyclopedia of virology, 3rd ed. Edited by B.W.J. Mahy and M.H.V. van Regenmortel. Elsevier, Oxford. pp. 125133.CrossRefGoogle Scholar
Farrar, R.R.Ridgway, R.L. 2000. Host plant effects on the activity of selected nuclear polyhedrosis viruses against the corn earworm and beet armyworm (Lepidoptera: Noctuidae). Environmental Entomology, 29: 108115.CrossRefGoogle Scholar
Federici, B.A. 1997. Baculovirus pathogenesis. In The baculoviruses. Edited by L.K. Miller. Plenum Press, New York. 447pp.Google Scholar
Felton, G.W.Duffey, S.S. 1990. Inactivation of a baculovirus by quinones formed in insect-damaged plant tissue. Journal of Chemical Ecology, 16: 12111236.CrossRefGoogle Scholar
Foster, M.A., Schultz, J.C., Hunter, M.D. 1992. Modelling gypsy moth–virus–leaf chemistry interactions: implications of plant quality for pest and pathogen dynamics. Journal of Animal Ecology, 61: 509520.CrossRefGoogle Scholar
Fox, L.R.Morrow, P.A. 1971. Specialization: species property or local phenomenon. Science, 211: 887893.CrossRefGoogle Scholar
Frost, P.C., Ebert, D., Smith, V.H. 2008. Responses of a bacterial pathogen to phosphorus limitation of its aquatic invertebrate host. Ecology, 89: 313318.CrossRefGoogle ScholarPubMed
Glynn, C., Herms, D.A., Egawa, M., Hansen, R., Mattson, W.J. 2003. Effects of nutrient availability on biomass allocation as well as constitutive and rapid induced herbivore resistance in poplar. Oikos, 101: 385397.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: 9991007.CrossRefGoogle ScholarPubMed
Hunter, M.D.Schultz, J.C. 1993. Induced plant defenses breached? Phytochemical induction protects an herbivore from disease. Oecologia, 94: 195203.CrossRefGoogle ScholarPubMed
Isaacs, R.van Timmeren, S. 2009. Monitoring and temperature-based prediction of the whitemarked tussock moth (Lepidoptera: Lymantriidae) in blueberry. Horticultural Entomology, 102: 637645.Google ScholarPubMed
Johns, R., Quiring, D.T., Lapointe, R., Lucarotti, C.J. 2009. Foliage-age mixing within balsam fir increases the fitness of a generalist caterpillar. Ecological Entomology, 34: 624631.CrossRefGoogle Scholar
Karowe, D.N. 1989. Differential effect of tannic acid on two tree-feeding Lepidoptera: implications for theories of plant anti-herbivore chemistry. Oecologia, 80: 506512.CrossRefGoogle ScholarPubMed
Keating, S.T.Yendol, W.G. 1987. Influence of selected host plants on gypsy moth (Lepidoptera: Lymantriidae) larval mortality caused by a baculovirus. Environmental Entomology, 16: 459462.CrossRefGoogle Scholar
Kirkpatrick, B.A., Washburn, J.O., Engelhard, E.K., Volkman, L.E. 1994. Primary infection of insect tracheae by Autographa californica M nuclear polyhedrosis virus. Virology, 203: 184186.CrossRefGoogle ScholarPubMed
Kopper, B.J., Lindroth, R.L., Nordheim, E.V. 2001. CO2 and O3 effects on paper birch (Betulaceae: Betula papyrifera) phytochemistry and whitemarked tussock moth (Lymantriidae: Orgyia leucostigma) performance. Population Ecology, 30: 11191126.Google Scholar
Lacey, L.A., Frutos, R., Kaya, H.K., Vail, P. 2001. Insect pathogens as biological control agents: do they have a future? Biological Control, 21: 230248.CrossRefGoogle Scholar
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: Biology, 273: 823829.Google Scholar
Li, H.Bonning, B.C. 2007. Evaluation of the insecticidal efficacy of wild-type and recombinant baculoviruses. In Baculovirus and insect cell expression protocols. Edited by D. Murhammer. Humana Press, Totowa, New Jersey. pp. 379404.Google Scholar
Lindroth, R.L., Kopper, B.J., Parsons, W.F.J., Bockheim, J.G., Karnosky, D.F., Hendrey, G.R., et al. 2001. Consequences of elevated carbon dioxide and ozone for foliar chemical composition and dynamics in trembling aspen (Populus tremuloides) and paper birch (Betula papryifera). Environmental Pollution, 115: 395404.CrossRefGoogle ScholarPubMed
Martineau, R. 1984. Insects harmful to forest trees. Multiscience Publications Ltd., Montreal.Google Scholar
Means, J.C.Passarelli, A.L. 2010. Viral fibroblast growth factor, matrix metalloproteases, and caspases are associated with enhancing systemic infection by baculoviruses. Proceedings of the National Academy of Sciences of the United States of America, 107: 98259830.CrossRefGoogle ScholarPubMed
Moreau, G., Lucarotti, C.J., Kettela, E.G., Thurston, G.S., Holmes, S., Weaver, C., et al. 2005. Aerial application of nucleopolyhedrovirus induces decline in increasing and peaking populations of Neodiprion abietis. Biological Control, 33: 6573.CrossRefGoogle Scholar
O'Reilly, D.R., Miller, L.K., Luckow, V.A. 1992. Baculovirus expression vectors: a laboratory manual. W. H. Freeman and Company, New York.Google Scholar
Passarelli, A.L. 2011. Barriers to success: how baculoviruses establish efficient systemic infections. Virology, 411: 383392.CrossRefGoogle ScholarPubMed
Renecker, L.A.Hudson, R.J. 1988. Seasonal quality of forages used by moose in the aspen-dominated boreal forest, central Alberta. Holarctic Ecology, 11: 111118.Google Scholar
Robbins, C.T., Hanley, T.A., Hagerman, A.E., Hjeljord, O., Baker, D.L., Schwartz, C.C., et al. 1987. Role of tannins in defending plants against ruminants: reduction in protein availability. Ecology, 68: 98107.CrossRefGoogle Scholar
Rose, A.H.Lindquist, O.H. 1997. Insects of eastern hardwood trees. Natural Resources Canada, Canadian Forest Service – Northern Forestry Centre, Forestry Technical Report, 29: 7273.Google Scholar
SAS Institute 1999. SAS/STAT user's guide, version 8. SAS Institute, Cary, North Carolina, USA.Google Scholar
Shikano, I., Ericsson, J.D., Cory, J.S., Myers, J.H. 2010. Indirect plant-mediated effects on insect immunity and disease resistance in a tritrophic system. Basic and Applied Ecology, 11: 1522.CrossRefGoogle Scholar
Stevenson, P.C., D'Cunha, R.F., Grzywacz, D. 2010. Inactivation of baculovirus by isoflavonoids on chickpea (Cicer arietinum) leaf surfaces reduces the efficacy of nucleopolyhedrovirus against Helicoverpa armigera. Journal of Chemical Ecology, 36: 227235.CrossRefGoogle ScholarPubMed
Szewczyk, B., Hoyos-Carvajal, L., Paluszek, M., Skrzecz, I., Lobo de Souza, M. 2006. Baculoviruses – re-emerging biopesticides. Biotechnology Advances, 24: 143160.CrossRefGoogle ScholarPubMed
Thurston, G.S.MacGregor, J.D. 2003. Body size – realized fecundity relationship of whitemarked tussock moth. The Canadian Entomologist, 135: 583586.CrossRefGoogle Scholar
Trudeau, D., Washburn, J.O., Volkman, L.E. 2001. Central role of hemocytes in Autographa californica M nucleopolyhedrovirus pathogenesis in Heliothis virescens and Helicoverpa zea. Journal of Virology, 75: 9961003.CrossRefGoogle ScholarPubMed
van Frankenhuyzen, K.E., Thurston, G., Lucarotti, C., Royama, T., Guscott, R., Georgeson, E., et al. 2002. Incidence and impact of Entomophaga aulicae (Zygomycetes: Entomophtorales) and a nucleopolyhedrovirus in an outbreak of the whitemarked tussock moth (Lepidoptera: Lymantriidae). The Canadian Entomologist, 134: 825845.CrossRefGoogle Scholar
Velioglu, Y.S., Mazza, G., Gao, L., Oomah, B.D. 1998. Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products. Journal of Agricultural Food Chemistry, 46: 41134117.CrossRefGoogle Scholar
Washburn, J.O., Kirkpatrick, B.A., Volkman, L.E. 1996. Insect protection against viruses. Nature, 383: 767.CrossRefGoogle Scholar