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Mutual interactions between an invasive bark beetle and its associated fungi

Published online by Cambridge University Press:  22 July 2011

B. Wang ,
C. Salcedo ,
M. Lu  and
J. Sun
B. Wang
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China Graduate School, Chinese Academy of Sciences, Beijing, 100049, China
C. Salcedo
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China
M. Lu
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China
J. Sun*
Affiliation:
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China
*
*Author for correspondence Fax: 86-10-6480 7099 E-mail: sunjh@ioz.ac.cn
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Abstract

Interactions between invasive insects and their fungal associates have important effects on the behavior, reproductive success, population dynamics and evolution of the organisms involved. The red turpentine beetle (RTB), Dendroctonus valens LeConte (Coleoptera: Scolytinae), an invasive forest pest in China, is closely associated with fungi. By carrying fungi on specialized structures in the exoskeleton, RTB inoculates fungi in the phloem of pines (when females dig galleries for egg laying and when males join them for mating). After eggs hatch, larvae gregariously feed on the phloem colonized by the fungi. We examined the effects of five isolates of RTB associated fungi (two from North America, Leptographium terebrantis and L. procerum, and three from China, Ophiostoma minus, L. sinoprocerum and L. procerum) on larval feeding activity, development and mortality. We also studied the effects of volatile chemicals produced in the beetle hindgut on fungal growth. Ophiostoma minus impaired feeding activity and reduced weight in RTB larvae. Leptographium sinoprocerum, L. terebrantis and L. procerum did not dramatically influence larval feeding and development compared to fungi-free controls. Larval mortality was not influenced by any of the tested fungi. Hindgut volatiles of RTB larvae, verbenol, myrtenol and myrtenal, inhibited growth rate of all the fungi. Our results not only show that D. valens associated fungus, O. minus, can be detrimental to its larvae; but, most importantly, they also show that these notorious beetles have an outstanding adaptive response evidenced by the ability to produce volatiles that inhibit growth of harmful fungus.

Keywords

antagonisminvasive insectinsect-fungus interactionsDendroctonus valensOphiostoma minusLeptographium spp.
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 102 , Issue 1 , February 2012 , pp. 71 - 77
Copyright
Copyright © Cambridge University Press 2011

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References

Aanen, D.K., Eggleton, P., Rouland-Lefevre, C., Guldberg-Froslev, T., Rosendahl, S. & Boomsma, J.J. (2002) The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proceedings of the National Academy of Sciences of the United States of America 99, 14887–14892.Google Scholar
Callaway, R.M. & Aschehoug, E.T. (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290, 521–523.CrossRefGoogle Scholar
Chapela, I.H., Rehner, S.A., Schultz, T.R. & Mueller, U.G. (1994) Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266, 1691–1694.CrossRefGoogle ScholarPubMed
Elton, C.S. (1958) The Ecology of Invasions by Animals and Plants. Chicago, IL, USA, The University of Chicago Press.CrossRefGoogle Scholar
Farrell, B.D., Sequeira, A.S., O'Meara, B.C., Normark, B.B., Chung, J.H. & Jordal, B.H. (2001) The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55, 2011–2027.Google Scholar
Fernandez, C., Monnier, Y., Ormeno, E., Baldy, V., Greff, S., Pasqualini, V., Mevy, J.P. & Bousquet-Melou, A. (2009) Variations in allelochemical composition of leachates of different organs and maturity stages of Pinus halepensis. Journal of Chemical Ecology 35, 970–979.Google Scholar
Harrington, T.C. & Cobb, F.W. Jr (1983) Pathogenicity of Leptographium and Verticicladiella spp. isolated from roots of western North American conifers. Phytopathology 73, 596–599.CrossRefGoogle Scholar
Hofstetter, R.W., Mahfouz, J.B., Klepzig, K.D. & Ayres, M.P. (2005) Effects of tree phytochemistry on the interactions among endophloedic fungi associated with the southern pine beetle. Journal of Chemical Ecology 31, 539–560.CrossRefGoogle ScholarPubMed
Hofstetter, R., Cronin, J., Klepzig, K., Moser, J. & Ayres, M. (2006) Antagonisms, mutualisms and commensalisms affect outbreak dynamics of the southern pine beetle. Oecologia 147, 679–691.CrossRefGoogle ScholarPubMed
Human, K.G. & Gordon, D.M. (1996) Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species. Oecologia 105, 405–412.Google Scholar
Hunt, C.E. & Yamada, S.B. (2003) Biotic resistance experienced by an invasive crustacean in a temperate estuary. Biological Invasions 5, 33–43.CrossRefGoogle Scholar
Jiu, M., Zhou, X.-P., Tong, L., Xu, J., Yang, X., Wan, F.-H. & Liu, S.-S. (2007) Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS ONE 2, e182.CrossRefGoogle ScholarPubMed
Kopper, B.J., Illman, B.L., Kersten, P.J., Klepzig, K.D. & Raffa, K.F. (2005) Effects of diterpene acids on components of a conifer bark beetle–fungal interaction: tolerance by Ips pini and sensitivity by its associate Ophiostoma ips. Environmental Entomology 34, 486–493.CrossRefGoogle Scholar
Levine, J.M., Adler, P.B. & Yelenik, S.G. (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecology Letters 7, 975–989.Google Scholar
Li, J.S., Chang, G.B., Song, Y.S., Wang, Y.W. & Chang, B.S. (2001) Control project on red turpentine beetle (Dendroctonus valens). Forest Pest Disease 4, 41–44 (in Chinese).Google Scholar
Lu, M., Zhou, X.D., De Beer, Z.W., Wingfield, M.J. & Sun, J.-H. (2009a) Ophiostomatoid fungi associated with the invasive pine-infesting bark beetle, Dendroctonus valens, in China. Fungal Diversity 38, 133–145.Google Scholar
Lu, M., Wingfield, M.J., Gillette, N.E., Mori, S.R. & Sun, J.-H. (2010) Complex interactions among host pines and fungi vectored by an invasive bark beetle. New Phytologist 187, 859–866.Google Scholar
Lu, Q., Decock, C., Zhang, X.Y. & Maraite, H. (2008) Leptographium sinoprocerum sp. nov., an undescribed species associated with Pinus tabuliformis-Dendroctonus valens in northern China. Mycologia 100, 275–290.CrossRefGoogle ScholarPubMed
Lu, Q., Decock, C., Zhang, X. & Maraite, H. (2009b) Ophiostomatoid fungi (Ascomycota) associated with Pinus tabuliformis infested by Dendroctonus valens (Coleoptera) in northern China and an assessment of their pathogenicity on mature trees. Antonie van Leeuwenhoek 96, 275–293.CrossRefGoogle Scholar
Luxova, A., Graves, A.D., Gries, R., Hamud, S.M. & Seybold, S.J. (2007) Frontalin: Production and response to an aggregation pheromone component by the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Scolytidae). pp. 13–17 in Abstract Presentations of 2007 Blodgett Forest Research Workshop. 2 February 2007, Georgetown, California.Google Scholar
Madelin, M.F. (1966) Fungal parasites of insects. Annual Review of Entomology 11, 423–448.CrossRefGoogle ScholarPubMed
McGlone, C., Sieg, C. & Kolb, T. (2011) Invasion resistance and persistence: established plants win, even with disturbance and high propagule pressure. Biological Invasions 13, 291–304.CrossRefGoogle Scholar
Mills, M.D., Rader, R.B. & Belk, M.C. (2004) Complex interactions between native and invasive fish: the simultaneous effects of multiple negative interactions. Oecologia 141, 713–721.Google Scholar
Owen, D.R., Lindahl, K.D., Wood, D.L. & Parmeter, J.R. Jr (1987) Pathogenicity of fungi isolated from Dendroctonus valens, D. brevicomis, and D. ponderosae to ponderosa pine seedlings. Phytopathology 77, 631–636.CrossRefGoogle Scholar
Parker, J.D. & Hay, M.E. (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecology Letters 8, 959–967.CrossRefGoogle ScholarPubMed
Renwick, J.A.A., Hughes, P.R. & Ty, T.D. (1973) Oxidation products of pinene in the bark beetle, Dendroctonus frontalis. Journal of Insect Physiology 19, 1735–1740.Google Scholar
Rodriguez, L. (2006) Can invasive species facilitate native species? evidence of how, when, and why these impacts occur. Biological Invasions 8, 927–939.Google Scholar
Rosner, B. & Sun, S.-G. (2004) Hypothesis testing: categorical data. pp. 374–383in Rosner, B. & Sun, S.-G. (Eds) Fundamentals of Biostatistics. Beijing, CHN, Science Press (in Chinese).Google Scholar
Shi, Z.H. & Sun, J.-H. (2009) Quantitative variation and biosynthesis of hindgut volatiles associated with the red turpentine beetle, Dendroctonus valens LeConte, at different attack phases. Bulletin of Entomological Research 100, 273–277.CrossRefGoogle ScholarPubMed
Smith, R.H. (1971) Red Turpentine Beetle. US Department of Agriculture Forest Pest Leaflet 55, 8.Google Scholar
Wallin, K.F. & Raffa, K.F. (2000) Influences of host chemicals and internal physiology on the multiple steps of postlanding host acceptance behaviour of Ips pini (Coleoptera: Scolytidae). Environmental Entomology 29, 442–453.Google Scholar
Wingfield, M.J. (1983) Association of Verticicladiella procera and Leptographium terrebrantis with insects in the Lake States. Canadian Journal of Forest Research 13, 1238–1245.CrossRefGoogle Scholar
Yan, Z., Sun, J.-H., Don, O. & Zhang, Z. (2005) The red turpentine beetle, Dendroctonus valens LeConte (Scolytidae): an exotic invasive pest of pine in China. Biodiversity and Conservation 14, 1735–1760.Google Scholar
Zhang, L. & Sun, J.-H. (2006) Electrophysiological and behavioral responses of Dendroctonus valens (Coleoptera: Curculionidae: Scolytinae) to candidate pheromone components identified in hindgut extracts. Environmental Entomology 35, 1232–1237.CrossRefGoogle Scholar
Zhang, L., Chen, Q. & Zhang, X. (2002) Studies on the morphological characters and bionomics of Dendroctonus valens LeConte. Scientia Silvae Sinicae 38, 95–99 (in Chinese).Google Scholar
Zhang, L., Sun, J.-H. & Clarke, S.R. (2006) Effects of verbenone dose and enantiomer on the interruption of response of the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Scolytidae), to its kariomones. Environmental Entomology 35, 655–660.Google Scholar