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What’s killing the green menace: mortality factors affecting the emerald ash borer (Coleoptera: Buprestidae) in North America?

Published online by Cambridge University Press:  10 November 2014

D. Barry Lyons
D. Barry Lyons*
Affiliation:
Natural Resources Canada, Canadian Forest Service, 1219 Queen Street East, Sault Ste. Marie, Ontario, Canada P6A 2E5
*
1Corresponding author (e-mail: [email protected]).
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Abstract

Emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), is an Asian species that was introduced into North America in the mid-1990s. The beetle has the potential to devastate populations of Fraxinus Linnaeus (Oleaceae) species. Several species of Hymenoptera parasitoids have made the transition from North American Agrilus Curtis hosts to A. planipennis, and some (e.g., Atanycolus Förster (Hymenoptera: Braconidae) species) have caused substantial mortality. Invertebrate predators of A. planipennis have been poorly investigated. Predation by woodpeckers (Aves: Picidae) has had the greatest impact on A. planipennis populations. Native entomopathogens have also been observed in populations of A. planipennis and are being explored as potential biological control agents. Agrilus planipennis is a freeze-intolerant species and as such perishes when its tissues freeze. However, the beetle can achieve a mean supercooling point of −30 °C by the production of cryoprotectants, especially glycerol. This low supercooling point in combination with temperatures higher than ambient in its overwintering microhabitat means that it can survive in most of its invaded range. As its distribution expands northward its cold hardiness may be challenged. North American species of Fraxinus possess some resistance to A. planipennis via defensive mechanisms, but these are quickly overcome by expanding larval populations. Intraspecific competition (via cannibalism and starvation) impacts larval survival.

Type
Original Article
Information
The Canadian Entomologist , Volume 147 , Special Issue 3: Emerald Ash Borer , June 2015 , pp. 263 - 276
Copyright
© Her Majesty the Queen in Right of Canada, as represented by Natural Resources Canada, Canadian Forest Service 2014 

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Footnotes

Subject editor: Krista Ryall

References

Abell, K.J., Duan, J.J., Bauer, L., Lelito, J.P., and Van Driesche, R.G. 2012. The effect of bark thickness on host partitioning between Tetrastichus planipennisi (Hymen: Eulophidae) and Atanycolus spp. (Hymen: Braconidae), two parasitoids of emerald ash borer (Coleop: Buprestidae). Biological Control, 63: 320–325.CrossRefGoogle Scholar
Akers, R.C. and Nielsen, D.G. 1990. Spatial emergence pattern of bronze birch borer, (Coleoptera: Buprestdae) from European white birch. Journal of Entomological Science, 25: 150–157.CrossRefGoogle Scholar
Anderson, R.F. 1944. The relation between host condition and attacks by the bronze birch borer. Journal of Economic Entomology, 37: 588–596.CrossRefGoogle Scholar
Anulewicz, A.C., McCullough, D.G., and Cappaert, D.L. 2007. Emerald ash borer (Agrilus planipennis) density and canopy dieback in three North American ash species. Arboriculture & Urban Forestry, 33: 338–349.CrossRefGoogle Scholar
Bale, J.S. 2002. Insects and low temperatures: from molecular biology to distributions and abundance. Philosophical Transactions of the Royal Society of London B, 357: 849–862.CrossRefGoogle ScholarPubMed
Baranchikov, Y., Mozolevskaya, E., Yurchenko, G., and Kenis, M. 2008. Occurrence of the emerald ash borer, Agrilus planipennis in Russia and its potential impact on European forestry. European and Mediterranean Plant Protection Organization Bulletin, 38: 233–238.Google Scholar
Barter, G.W. 1965. Survival and development of the bronze poplar borer Agrilus liragus Barter & Brown (Coleoptera: Buprestidae). The Canadian Entomologist, 97: 1063–1068.CrossRefGoogle Scholar
Bauer, L.S., Liu, H.-P., Gould, J.R., and Reardon, R.C. 2007. Progress on biological control of the emerald ash borer in North America. Biocontrol News and Information, 28: 51N–54N.Google Scholar
Bauer, L.S., Liu, H., Haack, R.A., Petrice, T.R., and Miller, D.L. 2004. Natural enemies of emerald ash borer in southeastern Michigan. In Emerald ash borer research and technology development meeting, 30 September–1 October 2004, Port Huron, Michigan, United States of America. Compiled by V. Mastro and R. Reardon. United States Department of Agriculture, Morgantown, West Virginia, United States of America. Pp. 33–34.Google Scholar
Burks, B.D. 1979. Family Eupelmidae. In Catalog of Hymenoptera in America north of Mexico. Volume 1, Symphyta and Apocrita (Parasitica). Edited by K.V. Krombein, P.D. Hurd, Jr., D.R. Smith, and B.D. Burks. Smithsonian Institution Press, Washington, District of Columbia, United States of America. Pp. 878–889.Google Scholar
Cappaert, D. and McCullough, D.G. 2009. Occurrence and seasonal abundance of Atanycolus cappaerti (Hymenoptera: Braconidae) a native parasitoid of emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae). Great Lakes Entomologist, 42: 16–29.Google Scholar
Cappaert, D., McCullough, D.G., Poland, T.M., and Siegert, N.W. 2005. Emerald ash borer in North America: a research and regulatory challenge. American Entomologist, 51: 152–165.CrossRefGoogle Scholar
Careless, P., Marshall, S.A., and Gill, B.D. 2013. The use of Cerceris fumipennis (Hymenoptera: Crabronidae) for surveying and monitoring emerald ash borer (Coleoptera: Buprestidae) infestations in eastern North America. The Canadian Entomologist, 146: 90–105.CrossRefGoogle Scholar
Careless, P.D., Marshall, S.A., Gill, B.D., Appleton, E., Favrin, R., and Kimoto, T. 2009. Cerceris fumipennis – a biosurveillance tool for emerald ash borer. Canadian Food Inspection Agency, Ottawa, Ontario, Canada.Google Scholar
Castrillo, L.A., Bauer, L.S., Liu, H., Griggs, M.H., and Vandenberg, J.D. 2010. Characterization of Beauveria bassiana (Ascomycota: Hypocreales) isolates associated with Agrilus planipennis (Coleoptera: Buprestidae) populations in Michigan. Biological Control, 54: 135–140.CrossRefGoogle Scholar
Chen, Y., Ciaramitaro, T., and Poland, T.M. 2011. Moisture content and nutrition as selection forces for emerald ash borer larval feeding behaviour. Ecological Entomology, 36: 344–354.CrossRefGoogle Scholar
Cipollini, D., Wang, Q., Whitehall, J.G.A., Powell, J.R., Bonello, P., and Herms, D.A. 2011. Distinguishing defensive characteristics in the phloem of ash species resistant and susceptible to emerald ash borer. Journal of Chemical Ecology, 37: 450–459.CrossRefGoogle ScholarPubMed
Crosthwaite, J.C., Sobek, S., Lyons, D.B., Bernards, M.A., and Sinclair, B.J. 2011. The overwintering physiology of the emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae). Journal of Insect Physiology, 57: 166–173.CrossRefGoogle ScholarPubMed
Dean, K.M., Vandenberg, J.D., Griggs, M.H., Bauer, L.S., and Fierke, M.K. 2012. Susceptibility of two hymenopteran parasitoids of Agrilus planipennis (Coleoptera: Buprestidae) to the entomopathogenic fungus Beauveria bassiana (Ascomycota: Hypocreales). Journal of Invertebrate Pathology, 109: 303–306.CrossRefGoogle Scholar
DeSantis, R.D., Moser, W.K., Gormanson, D.D., Bartlett, M.G., and Vermunt, B. 2013. Effects of climate on emerald ash borer mortality and the potential for ash survival in North America. Agricultural and Forest Meteorology, 178–179: 120–128.CrossRefGoogle Scholar
Dodds, H.D. and Otis, G. 2009. Breeding birds of mature woodlands of Point Pelee National Park prior to infestation by emerald ash borer, Agrilus planipennis. The Canadian Field-Naturalist, 123: 99–106.CrossRefGoogle Scholar
Duan, J.J., Abell, K.J., Bauer, L.S., Gould, J.R., and Van Driesche, R. 2014. Natural enemies implicated in the regulation of an invasive pest: a life table analysis of the population dynamics of the emerald ash borer. Agricultural and Forest Entomology. doi:10.1111/afe.12070.CrossRefGoogle Scholar
Duan, J.J., Bauer, L.S., Abell, K.J., and Van Driesche, R. 2012b. Population responses of hymenopteran parasitoids to the emerald ash borer (Coleoptera: Buprestidae) in recently invaded areas in north central United States. BioControl, 57: 199–209.CrossRefGoogle Scholar
Duan, J.J., Bauer, L.S., Ulyshen, M.D., Gould, J.R., and Van Driesche, R. 2011a. Development of methods for the field evaluation of Oobius agrili (Hymenoptera: Encyrtidae) in North America, a newly introduced egg parasitoid of the emerald ash borer (Coleoptera: Buprestidae). Biological Control, 56: 170–174.CrossRefGoogle Scholar
Duan, J.J., Fuester, R.W., Wildonger, J., Taylor, P.B., Barth, S., and Spichiger, S.E. 2009. Parasitoids attacking the emerald ash borer (Coleoptera: Buprestidae) in western Pennsylvania. Florida Entomologist, 92: 588–592.Google Scholar
Duan, J.J., Larson, K., Watt, T., Gould, J., and Lelito, J.P. 2013a. Effects of host plant and larval density on intraspecific competition in larvae of the emerald ash borer (Coleoptera: Buprestidae). Environmental Entomology, 42: 1193–1200.CrossRefGoogle ScholarPubMed
Duan, J.J., Taylor, P.B., and Fuester, R.W. 2011b. Biology and life history of Balcha indica, an ectoparasitoid attacking the emerald ash borer, Agrilus planipennis, in North America. Journal of Insect Science, 11: Article 127.CrossRefGoogle ScholarPubMed
Duan, J.J., Taylor, P.B., Fuester, R.W., Kula, R.R., and Marsh, P.M. 2013b. Hymenopteran parasitoids attacking the invasive emerald ash borer (Coleoptera: Buprestidae) in western and central Pennsylvania. Florida Entomologist, 96: 166–172.CrossRefGoogle Scholar
Duan, J.J., Ulyshen, M.D., Bauer, L.S., Gould, J., and Van Driesche, R. 2010. Measuring the impact of biotic factors on populations of immature emerald ash borers (Coleoptera: Buprestidae). Environmental Entomology, 103: 1513–1522.CrossRefGoogle Scholar
Duan, J.J., Yurchenko, G., and Fuester, R. 2012a. Occurrence of emerald ash borer (Coleoptera: Buprestidae) and biotic factors affecting its immature stages in the Russian Far East. Environmental Entomology, 41: 245–254.CrossRefGoogle ScholarPubMed
Dunn, J.P., Kimmerer, T.W., and Nordin, G.L. 1986. The role of host tree condition in attack of white oaks by the two lined chestnut borer, Agrilus bilineatus (Weber) (Coleoptera: Buprestidae). Oecologia, 70: 596–600.CrossRefGoogle Scholar
Eyles, A., Jones, W., Riedl, K., Cipollini, D., Schwartz, S., Chan, K., et al. 2007. Comparative phloem chemistry of Manchurian (Fraxinus mandshurica) and two North American ash species (Fraxinus americana and Fraxinus pennsylvanica). Journal of Chemical Ecology, 33: 1430–1448.CrossRefGoogle ScholarPubMed
Fissore, C., McFadden, J.P., Nelson, K.C., Peters, E.B., Hobbie, S.E., King, J.Y., et al. 2012. Potential impacts of emerald ash borer invasion on biochemical and water cycling in residential landscapes across a metropolitan region. Urban Ecosystems, 15: 1015–1030.CrossRefGoogle Scholar
Flower, C.E., Knight, K.S., and Gonzalez-Meler, M.A. 2013. Impacts of the emerald ash borer (Agrilus planipennis Fairmaire) induced ash mortality on forest carbon cycling and successional dynamics in the eastern United States. Biological Invasions, 15: 931–944.CrossRefGoogle Scholar
Flower, C.E., Long, L.C., Knight, K.S., Rebbeck, J., Brown, J.S., Gonzalez-Meler, M.A., et al. 2014. Native bark-foraging birds preferentially forage in infected ash (Fraxinus spp.) and prove effective predators of the invasive emerald ash borer (Agrilus planipennis Fairmaire). Forest Ecology and Management, 313: 300–306.CrossRefGoogle Scholar
Gandhi, K.J.K. and Herms, D.A. 2010a. Direct and indirect effects of alien insect hebivores on ecological processes and interactions in forests of eastern North America. Biological Invasions, 12: 389–405.CrossRefGoogle Scholar
Gandhi, K.J.K. and Herms, D.A. 2010b. North American arthropods at risk due to widespread Fraxinus mortality caused by the alien emerald ash borer. Biological Invasions, 12: 1839–1846.CrossRefGoogle Scholar
Gibson, G.A.P. 2005. The world species of Balcha Walker (Hymenoptera: Chalcidoidea: Eupelmidae), parasitoids of wood-boring beetles. Zootaxa, 1033: 1–62.CrossRefGoogle Scholar
Haack, R.A., Benjamin, D.M., and Schuh, B.A. 1981. Observations on the biology of Phasgonophora sulcata (Hymenoptera: Chalcididae), a larval parasitoid of the two-lined chestnut borer, Agrilus bilineatus (Coleoptera: Buprestidae) in Wisconsin. Great Lakes Entomologist, 14: 113–116.Google Scholar
Haack, R.A., Jendek, E., Liu, H., Marchant, K.R., Petrice, T.R., Poland, T.M., et al. 2002. The emerald ash borer: a new exotic pest in North America. Newsletter of the Michigan Entomological Society, 47: 1–5.Google Scholar
Hausman, C.E., Jaeger, J.F., and Rocha, O.J. 2010. Impacts of the emerald ash borer (EAB) eradication and tree mortality: potential for a secondary spread of invasive plant species. Biological Invasions, 12: 2013–2023.CrossRefGoogle Scholar
Herms, D. and McCullough, D.G. 2014. Emerald ash borer invasion of North America: history, biology, ecology, impacts, and management. Annual Review of Entomology, 59: 13–30.CrossRefGoogle ScholarPubMed
Hill, A.L., Whitehill, G.A., Opiyo, S.O., Phelan, P.L., and Bonello, P. 2012. Nutritional attributes of ash (Fraxinus spp.) outer bark and phloem and their relationships to resistance against the emerald ash borer. Tree Physiology, 32: 1522–1532.CrossRefGoogle ScholarPubMed
Jennings, D.E., Gould, J.R., Vandenberg, J.D., Duan, J.J., and Shrewsbury, P.M. 2013. Quantifying the impact of woodpecker predation on population dynamics of the emerald ash borer (Agrilus planipennis). Public Library of Science One, 8: e83491.Google ScholarPubMed
Johny, S., Kyei-Poku, G., Gauthier, D., and van Frankenhuyzen, K. 2012a. Isolation and characterization of Isaria farinosa and Purpureocillium lilacinum associated with emerald ash borer, Agrilus planipennis in Canada. Biocontrol Science and Technology, 22: 723–732.CrossRefGoogle Scholar
Johny, S., Kyei-Poku, G., Gauthier, D., van Frankenhuyzen, K., and Krell, P.J. 2012b. Characterization and virulence of Beauveria spp. recovered from emerald ash borer in southwestern Ontario. Journal of Invertebrate Pathology, 111: 41–49.CrossRefGoogle ScholarPubMed
Koenig, W.D., Liebhold, A.M., Bonter, D.N., Hochachka, W.M., and Dickinson, J.L. 2013. Effects of the emerald ash borer invasion on four species of birds. Biological Invasions, 15: 2095–2103.CrossRefGoogle Scholar
Kovacs, K.F., Haight, R.G., McCullough, D.G., Mercader, R.J., Siegert, N.W., and Liebhold, A.M. 2010. Cost of potential emerald ash borer damage in U.S. communities, 2009–2019. Ecological Economics, 69: 569–578.CrossRefGoogle Scholar
Kovacs, K.F., Haight, R.G., Mercader, R.J., and McCullough, D.G. 2014. A bioeconomic analysis of an emerald ash borer invasion of an urban forest with multiple jurisdictions. Resource and Energy Economics, 36: 270–289.CrossRefGoogle Scholar
Kovacs, K.F., Mercader, R.J., Haight, R.G., Siegert, N.W., McCullough, D.G., and Liebhold, A.M. 2011. The influence of satellite populations of emerald ash borer on projected economic costs in U.S. communities, 2010–2020. Journal of Environmental Management, 92: 2170–2181.CrossRefGoogle ScholarPubMed
Kula, R.R., Knight, K.S., Rebbeck, J., Bauer, L.S., Cappaert, D.L., and Gandhi, K.J.K. 2010. Leluthia astigma (Ashmead) (Hymenoptera: Braconidae: Doryctinae) as a parasitoid of Agrilus planipennis Fairmaire (Coleoptera: Buprestidae: Agrilinae), with an assessment of host associations for Nearctic species of Leluthia Cameron. Proceedings of the Entomological Society of Washington, 112: 246–257.CrossRefGoogle Scholar
Kuhn, K.L., Duan, J.J., and Hopper, K.R. 2013. Next-generation genome sequencing and assembly provides tools for phylogenetics and identification of closely related species of Spathius, parasitoids of Agrilus planipennis (emerald ash borer). Biological Control, 66: 77–82.CrossRefGoogle Scholar
Kyei-Poku, G., Gauthier, D., Schwarz, R., and van Frankenhuyzen, K. 2011. Morphology, molecular characteristics and prevalence of a Cystosporogenes species (Microsporidia) isolated from Agrilus anxius (Coleoptera: Buprestidae). Journal of Invertebrate Pathology, 107: 1–10.CrossRefGoogle ScholarPubMed
Kyei-Poku, G. and Johny, S. 2013. Evaluation of indigenous Beauveria isolates as potential agents for emerald ash borer management and the development of a diagnostic marker to monitor a post-release isolate. International Organisation for Biological and Integrated Control-West Palaearctic Regional Section Bulletin, 90: 119–124.Google Scholar
Lee, R.E. Jr. 2010. A primer on insect cold-tolerance. In Low temperature biology of insects. Edited by D.L. Denlinger and R.E. Lee Jr. Cambridge University Press, New York, New York, United States of America. Pp. 3–34.CrossRefGoogle Scholar
Liang, L. and Fei, S. 2014. Divergence of the potential invasion range of emerald ash borer and its host distribution in North America under climate change. Climatic Change, 122: 735–746.CrossRefGoogle Scholar
Lindell, C.A., McCullough, D.G., Cappaert, D., Apostolou, N.M., and Roth, M.B. 2008. Factors influencing woodpecker predation on emerald ash borer. American Midland Naturalist, 159: 434–444.CrossRefGoogle Scholar
Liu, H., Bauer, L.S., Gao, R., Zhao, T., Petrice, T.R., and Haack, R.A. 2003. Exploratory survey for the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae), and its natural enemies in China. Great Lakes Entomologist, 36: 191–204.Google Scholar
Lyons, D.B. 2010. Biological control research update. In Workshop proceedings: guiding principles for managing the emerald ash borer in urban environments. Edited by D.B. Lyons and T.A. Scarr. Ontario Ministry of Natural Resources and Natural Resources Canada, Canadian Forest Service, Sault Ste. Marie, Ontario, Canada. Pp. 27–32.Google Scholar
Lyons, D.B., Lavallee, R., Kyei-Poku, G., van Frankenhuyzen, K., Johny, S., Guertin, C., et al. 2012. Towards the development of an autocontamination trap system to manage populations of emerald ash borer (Coleoptera: Buprestidae) with the native entompathogenic fungus, Beauveria bassiana. Journal of Economic Entomology, 105: 1929–1939.CrossRefGoogle Scholar
Marsh, P.M. 1979. Family Braconidae. In Catalog of Hymenoptera in America north of Mexico. Volume 1, Symphyta and Apocrita (Parasitica). Edited by K.V. Krombein, P.D. Hurd, Jr., D.R. Smith, and B.D. Burks. Smithsonian Institution Press, Washington, Distict of Columbia, United States of America. Pp. 144–295.Google Scholar
Marsh, P.M. and Strazanac, J.S. 2009. A taxonomic review of the genus Spathius Nees (Hymenoptera: Braconidae) in North America and comments on the biological control of the emerald ash borer (Coleoptera: Buprestidae). Journal of Hymenoptera Research, 18: 80–112.Google Scholar
Marsh, P.M., Strazanac, J.S., and Laurusonis, S.Y. 2009. Description of a new species of Atanycolus (Hymenoptera: Braconidae) from Michigan reared from the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae: Agrilinae). Great Lakes Entomologist, 42: 8–15.Google Scholar
Marshall, S.A., Paiero, S.M., and Buck, M. 2005. Buprestid sampling at nests of Cerceris fumipennis (Hymenoptera: Crabronidae) in southern Ontario: the first Canadian records of three buprestids (Coleoptera: Buprestidae). The Canadian Entomologist, 137: 416–419.CrossRefGoogle Scholar
McCullough, D.G. and Siegert, N.W. 2007. Estimating potential emerald ash borer (Coleoptera: Buprestidae) populations using ash inventory data. Journal of Economic Entomology, 100: 1566–1586.CrossRefGoogle ScholarPubMed
McKenney, D.W., Pedlar, J.H., Yemshanov, D., Lyons, D.B., Campbell, K.L., and Lawrence, K. 2012. Estimates of the potential cost of emerald ash borer (Agrilus planipennis Fairmaire) in Canadian municipalities. Arboriculture & Urban Forestry, 38: 81–91.CrossRefGoogle Scholar
Poland, T.M. and McCullough, D.G. 2006. Emerald ash borer: invasion of the urban forest and the threat to North America’s ash resource. Journal of Forestry, 104: 118–124.Google Scholar
Poland, T.M. and McCullough, D.G. 2010. SLAM: a multi-agency pilot project to SL.ow A.sh M.ortality caused by emerald ash borer in outlier sights. Newsletter of the Michigan Entomological Society, 55: 4–8.Google Scholar
Pureswaran, D.S. and Poland, T.M. 2009. Host selection and feeding preference of Agrilus planipennis (Coleoptera: Buprestidae) on ash (Fraxinus spp.). Environmental Entomology, 38: 757–765.CrossRefGoogle ScholarPubMed
Rebek, E.J., Herms, D.A., and Smitley, D.R. 2008. Interspecific variation in resistance to emerald ash borer (Coleoptera: Buprestidae) among North American and Asian ash (Fraxinus spp.). Environmental Entomology, 37: 242–246.CrossRefGoogle ScholarPubMed
Sabbahi, R., Lavallee, R., Merzouki, A., and Guertin, C. 2009. Differentiation of entomopathogenic fungus Beauveria bassiana (Ascomycetes: Hyprocreales) isolates by PCR-RFLP. Phytoprotection, 90: 49–56.CrossRefGoogle Scholar
Siegert, N.W., McCullough, D.G., Liebhold, A.M., and Telewski, F.W. 2014. Dendrochronological reconstruction of the epicentre and early spread of emerald ash borer in North America. Diversity and Distributions, 20: 847–859.CrossRefGoogle Scholar
Sobek-Swant, S., Crosthwaite, J.C., Lyons, D.B., and Sinclair, B.J. 2012a. Could phenotypic plasticity limit an invasive species? Incomplete reversibility of mid-winter deacclimation in emerald ash borer. Biological Invasions, 14: 115–125.CrossRefGoogle Scholar
Sobek-Swant, S., Kluza, D.A., Cuddington, K., and Lyons, D.B. 2012b. Potential distribution of emerald ash borer: what can we learn from ecological niche models using Maxent and GARP? Forest Ecology and Management, 281: 23–31.CrossRefGoogle Scholar
Tanis, S.R. and McCullough, D.G. 2012. Differential persistance of blue ash and white ash following emerald ash borer invasion. Canadian Journal Forest Research, 42: 1541–1550.CrossRefGoogle Scholar
Tluczek, A.R., McCullough, D.G., and Poland, T.M. 2011. Influence of host stress on emerald ash borer (Coleoptera: Buprestidae) adult density, development and distribution in Fraxinus pennsylvanica trees. Environmental Entomology, 40: 357–366.CrossRefGoogle Scholar
Vansanthakumar, A., Handelsman, J., Schloss, P.D., Bauer, L.S., and Raffa, K.F. 2008. Gut microbiota of an invasive subcortical beetle, Agrilus planipennis Fairmaire, across various life stages. Environmental Entomology, 37: 1344–1353.CrossRefGoogle Scholar
Vermunt, B., Cuddington, K., Sobek-Swant, S., and Crosthwaite, J. 2012a. Cold temperature and emerald ash borer: modelling the minimum under-bark temperature of ash trees in Canada. Ecological Modelling, 235–236: 19–25.CrossRefGoogle Scholar
Vermunt, B., Cuddington, K., Sobek-Swant, S., Crosthwaite, J.C., Lyons, D.B., and Sinclair, B.J. 2012b. Temperatures experienced by wood-boring beetles in the under-bark microclimate. Forest Ecology and Management, 269: 149–157.CrossRefGoogle Scholar
Wallander, E. 2008. Systematics of Fraxinus (Oleaceae) and evolution of dioecy. Plant Systematics and Evolution, 273: 25–49.CrossRefGoogle Scholar
Wang, X.-Y., Yang, Z.-Q., Gould, J.R., Zhang, Y.-N., Liu, G.-J., and Liu, E.-S. 2010. The biology and ecology of the emerald ash borer, Agrilus planipennis, in China. Journal of Insect Science, 10: Article 128.CrossRefGoogle ScholarPubMed
Wei, X., Wu, Y., Reardon, R., Sun, T.-H., Lu, M., and Sun, J.-H. 2007. Biology and damage traits of emerald ash borer (Agrilus planipennis Fairmaire) in China. Insect Science, 14: 367–373.CrossRefGoogle Scholar
Whitehill, J.G.A., Opiyo, S.O., Koch, J.L., Herms, D.A., Cipollini, D.F., and Bonello, P. 2012. Interspecific comparison of constitutive ash phloem phenolic chemistry reveals compounds unique to Manchurian ash, a species resistant to emerald ash borer. Journal of Chemical Ecology, 38: 499–511.CrossRefGoogle Scholar
Whitehill, J.G.A., Popova-Butler, A., Green-Church, K.B., Koch, J.L., Herms, D.A., and Bonello, P. 2011. Interspecific proteomic comparisons reveal ash phloem genes potentially involved in constitutive resistance to the emerald ash borer. Public Library of Science One, 6: e24863.Google ScholarPubMed
Wu, H., Li, M., Yang, Z., Wang, X., Wang, H., and Bai, L. 2007. Cold hardiness of Agrilus planipennis and its two parasitoids, Spathius agrili and Tetrastichus planipennisi. Chinese Journal of Biological Control, 23: 119–122.Google Scholar