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Assessment of the impact of symbiont Ophiostomatales (Fungi) on mountain pine beetle (Coleoptera: Curculionidae) performance on a jack pine (Pinaceae) diet using a novel in vitro rearing method

Published online by Cambridge University Press:  15 June 2015

Colin L. Myrholm  and
David W. Langor
Colin L. Myrholm
Affiliation:
Natural Resources Canada, Canadian Forest Service, 5320–122 St., Edmonton, Alberta, Canada T6H 3S6
David W. Langor*
Affiliation:
Natural Resources Canada, Canadian Forest Service, 5320–122 St., Edmonton, Alberta, Canada T6H 3S6
*
2 Corresponding author (e-mail: dlangor@nrcan.gc.ca).
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Abstract

A novel “rearing-tube” method was developed and used to investigate the performance of mountain pine beetle (MPB), Dendroctonus ponderosae Hopkins (Coleoptera: Curculionidae: Scolytinae), with its three main ophiostomatalean fungal symbionts, Grosmannia clavigera (Robinson-Jeffrey and Davidson) Zipfel, de Beer, and Wingfield (Ophiostomataceae), Ophiostoma montium (Rumbold) von Arx (Ophiostomataceae), and Leptographium longiclavatum Lee, Kim, and Breuil (Ophiostomataceae). Transparent glass tubes filled with sterile ground jack pine (Pinus banksiana Lambert; Pinaceae) phloem and sapwood (9:1 ratio) were used to rear MPB from egg to adult with each fungus under controlled environmental conditions. Mountain pine beetle mortality was higher and development longer in fungus-free controls compared to fungal treatments. Among fungal treatments, insects developed faster, constructed shorter larval galleries, and had fewer supernumerary instars with L. longiclavatum. Insect survival was not affected by fungal treatments. Hyphal extension through the rearing medium was fastest for L. longiclavatum. Phloem nitrogen was reduced significantly by the presence of L. longiclavatum. Results support the hypothesis that ophiostomatalean symbionts provide benefits to MPB. The rearing-tube method is useful to tease apart confounding interspecific interactions between bark beetles and symbiotic fungus species.

Type
Behaviour & Ecology
Information
The Canadian Entomologist , Volume 148 , Issue 1 , February 2016 , pp. 68 - 82
Copyright
© Her Majesty the Queen in Right of Canada, as represented by Natural Resources Canada 2015 

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Footnotes

Subject editor: Rob Johns

1

Shared primary authorship

References

Adams, A.S. and Six, D.L. 2007. Temporal variation in mycophagy and prevalence of fungi associated with developmental stages of Dendroctonus ponderosae . Environmental Entomology, 36: 64–72.Google Scholar
Addison, A.L., Powell, J.A., Six, D.L., Moore, M., and Bentz, B.J. 2013. The role of temperature variability in stabilizing the mountain pine beetle-fungus mutualism. Journal of Theoretical Biology, 335: 40–50.CrossRefGoogle ScholarPubMed
Aldarf, M., Amrane, A., and Prigent, Y. 2002. Carbon and nitrogen substrates consumption, ammonia release and proton transfer in relation with growth of Geotrichum candidum and Penicillium camambertii on a solid medium. Journal of Biotechnology, 95: 99–108.Google Scholar
Amman, G.D. 1972. Some factors affecting oviposition behaviour of the mountain pine beetle. Environmental Entomology, 1: 691–695.Google Scholar
Ayers, M.P., Wilkens, R.T., Ruel, J.J., Lombardero, M.J., and Vallery, E. 2000. Nitrogen budgets of phloem-feeding bark beetles with and without symbiotic fungi (Coleoptera: Scolytidae). Ecology, 81: 2198–2210.Google Scholar
Barras, S.J. 1972. Improved White’s solution for surface sterilization of pupae of Dendroctonus frontalis . Journal of Economic Entomology, 65: 1504.CrossRefGoogle ScholarPubMed
Barras, S.J. and Hodges, J.D. 1974. Weight, moisture and lipid changes during the life cycle of the southern pine beetle. Research Note SO-178. United States Department of Agricuture, Forest Service, New Orleans, Louisiana, United States of America.Google Scholar
Bentz, B.J. and Six, D.L. 2006. Ergosterol content of fungi associated with Dendroctonus ponderosae and Dendroctonus rufipennis (Coleoptera: Curculionidae, Scolytinae). Annals of the Entomological Society of America, 99: 189–194.Google Scholar
Bleiker, K.P., Potter, S.E., Lauzon, C.R., and Six, D.L. 2009. Transport of fungal symbionts by mountain pine beetles. The Canadian Entomologist, 141: 503–514.Google Scholar
Bleiker, K.P. and Six, D.L. 2007. Dietary benefits of fungal associates to an eruptive herbivore: potential implications of multiple associates on host population dynamics. Environmental Entomology, 36: 1384–1396.CrossRefGoogle Scholar
Bleiker, K.P. and Six, D.L. 2009a. Competition and coexistence in a multi-partner mutualism: interactions between two fungal symbionts of the mountain pine beetle in beetle-attacked trees. Microbial Ecology, 57: 191–202.Google Scholar
Bleiker, K.P. and Six, D.L. 2009b. Effects of water potential and solute on the growth and interactions of two fungal symbionts of the mountain pine beetle. Mycological Research, 113: 3–15.Google Scholar
Bollag, J.-M. and Tung, G. 1972. Nitrous oxide release by soil fungi. Soil Biology and Biochemistry, 4: 271–276.CrossRefGoogle Scholar
Cook, S.P., Shirley, B.M., and Zambino, P.J. 2010. Nitrogen concentration in mountain pine beetle larvae reflects nitrogen status of the tree host and two fungal associates. Environmental Entomology, 39: 821–826.Google Scholar
Cullingham, C.I., Cooke, J.E.K., Dang, S., Davis, C.S., Cooke, B.J., and Coltman, D.W. 2011. Mountain pine beetle host range expansion threatens the boreal forest. Molecular Ecology, 20: 2157–2171.Google Scholar
Dahlsten, D.L. and Stephen, F.M. 1974. Natural enemies and associates of the mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Scolytidae), in sugar pine. The Canadian Entomologist, 106: 1211–1217.Google Scholar
Douglas, A.E. 2009. The microbial dimension of insect nutritional ecology. Microbial Ecology, 23: 38–47.Google Scholar
Esperk, T., Tammaru, T., and Nylin, S. 2007. Intraspecific variability in number of larval instars in insects. Journal of Economic Entomology, 100: 627–645.CrossRefGoogle ScholarPubMed
Gibson, C.M. and Hunter, M.S. 2009. Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecology Letters, 13: 223–234.CrossRefGoogle ScholarPubMed
Goodsman, D.W., Erbilgen, N., and Lieffers, V.J. 2012. The impact of phloem nutrients on overwintering mountain pine beetles and their fungal symbionts. Environmental Entomology, 41: 478–486.Google Scholar
Heming, B.S. 2003. Insect development and evolution. Comstock Publishing Associates, Cornell University Press, Ithaca, New York, United States of America.Google Scholar
Iwata, R. and Nishimoto, K. 1984. Studies on the autecology of Lyctus brunneus (Stephens) (Coleoptera: Lyctidae) VI. Larval development and instars with special reference to an individual rearing method. Wood Research, 71: 32–45.Google Scholar
Kim, J.-J., Allen, E.A., Humble, L.M., and Breuil, C. 2005. Ophiostomoid and basidiomycetous fungi associated with green, red and grey lodgepole pines after mountain pine beetle (Dendroctonus ponderosae) infestation. Canadian Journal of Forest Research, 35: 274–284.Google Scholar
Klepzig, K.D. and Six, D.L. 2004. Bark beetle-fungal symbioses: context dependency in complex associations. Symbiosis, 37: 189–205.Google Scholar
Lee, S., Kim, J.-J., and Breuil, C. 2005. Leptographium longiclavatum sp. nov., a new species associated with the mountain pine beetle, Dendroctonus ponderosae . Mycological Research, 109: 1162–1170.CrossRefGoogle Scholar
Lee, S., Kim, J.-J., and Breuil, C. 2006a. Pathogenicity of Leptographium longiclavatum associated with Dendroctonus ponderosae to Pinus contorta . Canadian Journal of Forest Research, 36: 2864–2872.CrossRefGoogle Scholar
Lee, S., Kim, J.-J., and Breuil, C. 2006b. Diversity of fungi associated with the mountain pine beetle, Dendroctonus ponderosae and infested lodgepole pines in British Columbia. Fungal Diversity, 22: 91–105.Google Scholar
Martin, M.M. 1979. Biochemical implications of insect mycophagy. Biological Reviews, 54: 1–21.CrossRefGoogle Scholar
Massey, C.L. 1974. Biology and taxonomy of nematode parasites and associates of bark beetles in the United States. Agriculture Handbook 446. United States Department of Agricuture, Forest Service, Washington, District of Columbia, United States of America.Google Scholar
Mori, B.A., Proctor, H.C., Walter, D.E., and Evenden, M.L. 2011. Phoretic mite associates of mountain pine beetle at the leading edge of an infestation in northwestern Alberta. The Canadian Entomologist, 143: 44–55.Google Scholar
Nijhout, H.F. 1994. Insect hormones. Princeton University Press, Princeton, New Jersey, United States of America.CrossRefGoogle Scholar
Paine, T.D., Raffa, K.F., and Harrington, T.C. 1997. Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annual Review of Entomology, 42: 179–206.CrossRefGoogle ScholarPubMed
Reid, R.W. 1962a. Biology of the mountain pine beetle, Dendroctonus monticolae Hopkins, in the east Kootenay region of British Columbia. I. Life cycle, brood development, and flight periods. The Canadian Entomologist, 94: 531–538.Google Scholar
Reid, R.W. 1962b. Biology of the mountain pine beetle, Dendroctonus monticolae Hopkins, in the east Kootenay region of British Columbia. II. Behaviour in the host, fecundity, and internal changes in the female. The Canadian Entomologist, 94: 605–613.CrossRefGoogle Scholar
Reid, R.W. and Gates, H. 1970. Effect of temperature and resin on hatch of eggs of the mountain pine beetle (Dendroctonus ponderosae). The Canadian Entomologist, 102: 617–622.Google Scholar
Rice, A.V. and Langor, D.W. 2009. Mountain pine beetle-associated blue-stain fungi in lodgepole×jack pine hybrids near Grande Prairie, Alberta (Canada). Forest Pathology, 39: 323–334.CrossRefGoogle Scholar
Rice, A.V., Thormann, M.N., and Langor, D.W. 2007. Virulence of and interactions among mountain pine beetle-associated blue-stain fungi on two pine species and hybrids. Canadian Journal of Botany, 85: 316–323.Google Scholar
Rice, A.V., Thormann, M.N., and Langor, D.W. 2008. Mountain pine beetle-associated blue-stain fungi are differentially adapted to boreal temperatures. Forest Pathology, 38: 113–123.Google Scholar
Roe, A.D., James, P.M.A., Rice, R.V., Cooke, J.E.K., and Sperling, F.A.H. 2011. Spatial community structure of mountain pine beetle fungal symbionts across a latitudinal gradient. Microbial Ecology, 62: 347–360.CrossRefGoogle ScholarPubMed
Safranyik, L. 1976. Size- and sex-related emergence, and survival in cold storage, of mountain pine beetle adults. The Canadian Entomologist, 108: 209–212.CrossRefGoogle Scholar
Safranyik, L., Carroll, A.L., Régnière, J., Langor, D.W., Riel, W.G., Shore, T.L., et al. 2010. Potential for range expansion of the mountain pine beetle into the boreal forest of North America. The Canadian Entomologist, 142: 415–442.Google Scholar
Safranyik, L. and Linton, D.A. 1998. Mortality of mountain pine beetle larvae, Dendroctonus ponderosae (Coleoptera: Scolytidae) in logs of lodgepole pine (Pinus contorta var. latifolia) at constant low temperatures. Journal of the Entomological Society of British Columbia, 95: 81–97.Google Scholar
Shintani, Y., Munyiri, F., and Ishikawa, Y. 2003. Change in significance of feeding during larval development in the yellow-spotted longicorn beetle, Psacothea hilaris . Journal of Insect Physiology, 49: 975–981.CrossRefGoogle ScholarPubMed
Six, D.L. 2012. Ecological and evolutionary determinants of bark beetle – fungus symbioses. Insects, 3: 339–366.CrossRefGoogle ScholarPubMed
Six, D.L. and Bentz, B.J. 2007. Temperature determines symbiont abundance in a multipartite bark beetle-fungus ectosymbiosis. Microbial Ecology, 54: 112–118.Google Scholar
Six, D.L. and Klepzig, K.D. 2004. Dendroctonus bark beetles as model systems for studies on symbiosis. Symbiosis, 37: 207–232.Google Scholar
Six, D.L. and Paine, T.D. 1998. Effects of mycangial fungi and host tree species on progeny survival and emergence of Dendroctonus ponderosae (Coleoptera: Scolytidae). Environmental Entomology, 27: 1393–1401.Google Scholar
Solheim, H. 1995. Early stages of blue stain fungus invasion of lodgepole pine sapwood following mountain pine beetle attack. Canadian Journal of Botany, 73: 70–74.Google Scholar
Solheim, H. and Krokene, P. 1998. Growth and virulence of mountain pine beetle associated blue-stain fungi, Ophiostoma clavigerum and Ophiostoma montium . Canadian Journal of Botany, 76: 561–566.Google Scholar
Whitney, H.S. 1971. Association of Dendroctonus ponderosae (Coleoptera: Scolytidae) with blue stain fungi and yeasts during brood development in lodgepole pine. The Canadian Entomologist, 103: 1495–1503.Google Scholar
Whitney, H.S. and Farris, S.H. 1970. Maxillary mycangium in the mountain pine beetle. Science, 167: 54–55.Google Scholar
Winder, R.S., Macey, D.E., and Cortese, J. 2010. Dominant bacteria associated with broods of mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Curculionidae, Scolytinae). Journal of the Entomological Society of British Columbia, 107: 43–56.Google Scholar