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Biotic mortality factors affecting emerald ash borer (Agrilus planipennis) are highly dependent on life stage and host tree crown condition

  • D.E. Jennings (a1), J.J. Duan (a2) and P.M. Shrewsbury (a1)

Emerald ash borer (EAB), Agrilus planipennis, is a serious invasive forest pest in North America responsible for killing tens to hundreds of millions of ash trees since it was accidentally introduced in the 1990s. Although host-plant resistance and natural enemies are known to be important sources of mortality for EAB in Asia, less is known about the importance of different sources of mortality at recently colonized sites in the invaded range of EAB, and how these relate to host tree crown condition. To further our understanding of EAB population dynamics, we used a large-scale field experiment and life-table analyses to quantify the fates of EAB larvae and the relative importance of different biotic mortality factors at 12 recently colonized sites in Maryland. We found that the fates of larvae were highly dependent on EAB life stage and host tree crown condition. In relatively healthy trees (i.e., with a low EAB infestation) and for early instars, host tree resistance was the most important mortality factor. Conversely, in more unhealthy trees (i.e., with a moderate to high EAB infestation) and for later instars, parasitism and predation were the major sources of mortality. Life-table analyses also indicated how the lack of sufficient levels of host tree resistance and natural enemies contribute to rapid population growth of EAB at recently colonized sites. Our findings provide further evidence of the mechanisms by which EAB has been able to successfully establish and spread in North America.

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Abell K.J., Duan J.J., Bauer L., Lelito J.P. & 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, 320325.
Abell K.J., Bauer L.S., Duan J.J. & Van Driesche R. (2014) Long-term monitoring of the introduced emerald ash borer (Coleoptera: Buprestidae) egg parasitoid, Oobius agrili (Hymenoptera: Encyrtidae), in Michigan, USA and evaluation of a newly developed monitoring technique. Biological Control 79, 3642.
Aukema J.E., McCullough D.G., Von Holle B., Liebhold A.M., Britton K. & Frankel S.J. (2010) Historical accumulation of nonindigenous forest pests in the continental United States. Bioscience 60, 886897.
Aukema J.E., Leung B., Kovacs K., Chivers C., Britton K.O., Englin J., Frankel S.J., Haight R.G., Holmes T.P., Liebhold A.M., McCullough D.G. & Von Holle B. (2011) Economic impacts of non-native forest insects in the continental United States. PLoS ONE 6, e24587.
Bauer L.S., Liu H., Haack R.A., Gao R., Zhao T., Miller D.L. & Petrice T.R. (2005) Update on emerald ash borer natural enemy surveys in Michigan and China. pp. 7172 in Mastro V. & Reardon R. (Eds) Proceedings of the Emerald Ash Borer Research and Technology Development Meeting, Romulus, MI, 5–6 October 2004, Morgantown, West Virginia, USDA Forest Service.
Cappaert D., McCullouch D.G. & Poland T.M. (2005 a) Emerald ash borer life-cycle: a reassessment. pp. 1920 in Mastro V. & Reardon R. (Eds) Proceedings of the Emerald Ash Borer Research and Technology Development Meeting, Romulus, MI, 5–6 October 2004, Morgantown, West Virginia, USDA Forest Service.
Cappaert D., McCullough D.G., Poland T.M. & Siegert N.W. (2005 b) Emerald ash borer in North America: a research and regulatory challenge. American Entomologist 51, 152165.
Cappaert D., McCullouch D.G. & Poland T.M. (2005 c) The upside of the emerald ash borer catastrophe: a feast for woodpeckers. pp. 6970 in Mastro V. & Reardon R. (Eds) Proceedings of the Emerald Ash Borer Research and Technology Development Meeting, Romulus, MI, 5–6 October 2004, Morgantown, West Virginia, USDA Forest Service.
Cárdenas A.M. & Gallardo P. (2012) The effect of temperature on the preimaginal development of the Jewel beetle, Coraebus florentinus (Coleoptera: Buprestidae). European Journal of Entomology 109, 2128.
Duan J.J., Fuester R.W., Wildonger J., Taylor P.B., Barth S. & Spichiger S.E. (2009) Parasitoids attacking the emerald ash borer (Coleoptera: Buprestidae) in western Pennsylvania. Florida Entomologist 92, 588592.
Duan J.J., Ulyshen M.D., Bauer L.S., Gould J. & Van Driesche R. (2010) Measuring the impact of biotic factors on populations of immature emerald ash borers (Coleoptera: Buprestidae). Environmental Entomologist 39, 15131522.
Duan J.J., Yurchenko G. & Fuester R. (2012 a) Occurrence of emerald ash borer (Coleoptera: Buprestidae) and biotic factors affecting its immature stages in the Russian Far East. Environmental Entomologist 41, 245254.
Duan J.J., Bauer L.S., Abell K.J. & Van Driesche R. (2012 b) Population responses of hymenopteran parasitoids to the emerald ash borer (Coleoptera: Buprestidae) in recently invaded areas in north central United States. BioControl 57, 199209.
Duan J.J., Bauer L.S., Hansen J.A., Abell K.J. & Van Driesche R. (2012 c) An improved method for monitoring parasitism and establishment of Oobius agrili (Hymenoptera: Encyrtidae), an egg parasitoid introduced for biological control of the emerald ash borer (Coleoptera: Buprestidae) in North America. Biological Control 60, 255261.
Duan J.J., Bauer L.S., Abell K.J., Lelito J. & Van Driesche R. (2013 a) Establishment and abundance of Tetrastichus planipennisi (Hymenoptera: Eulophidae) in Michigan: potential for success in classical biocontrol of the invasive emerald ash borer (Coleoptera: Buprestidae). Journal of Economic Entomology 106, 11451154.
Duan J.J., Watt T., Taylor P., Larson K. & Lelito J.P. (2013 b) Effects of ambient temperature on egg and larval development of the invasive emerald ash borer (Coleoptera: Buprestidae): implications for laboratory rearing. Journal of Economic Entomology 106, 21012108.
Duan J.J., Larson K., Watt T., Gould J. & Lelito J.P. (2013 c) Effects of host plant and larval density on intraspecific competition in larvae of the emerald ash borer (Coleoptera: Buprestidae). Environmental Entomology 42, 11931200.
Duan J.J., Abell K.J., Bauer L.S., Gould J.R. & 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 16, 406416.
Flower C.E., Knight K.S. & Gonzalez-Meler M.A. (2013 a) Impacts of the emerald ash borer (Agrilus planipennis Fairmaire) induced ash (Fraxinus spp.) mortality on forest carbon cycling and successional dynamics in the eastern United States. Biological Invasions 15, 931944.
Flower C.E., Knight K.S., Rebbeck J. & Gonzalez-Meler M.A. (2013 b) The relationship between the emerald ash borer (Agrilus planipennis) and ash (Fraxinus spp.) tree decline: using visual canopy condition assessments and leaf isotope measurements to assess pest damage. Forest Ecology and Management 303, 143147.
Flower C.E., Long L.C., Knight K.S., Rebbeck J., Brown J.S., Gonzalez-Meler M.A. & Whelan C.J. (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, 300306.
Gandhi K.J.K. & Herms D.A. (2010 a) Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biological Invasions 12, 389405.
Gandhi K.J.K. & Herms D.A. (2010 b) North American arthropods at risk due to widespread Fraxinus mortality caused by the alien emerald ash borer. Biological Invasions 12, 18391846.
Gandhi K.J.K., Smith A., Hartzler D.M. & Herms D.A. (2014) Indirect effects of emerald ash borer-induced ash mortality and canopy gap formation on epigaeic beetles. Environmental Entomology 43, 546555.
Hanks L.M., Paine T.D. & Millar J.G. (2005) Influence of the larval environment on performance and adult body size of the wood-boring beetle Phoracantha semipunctata . Entomologia Experimentalis et Applicata 114, 2534.
Herms D.A. & McCullough D.G. (2014) Emerald ash borer invasion of North America: history, biology, ecology, impacts, and management. Annual Review of Entomology 59, 1330.
Holmes T.P., Aukema J.E., Von Holle B., Liebhold A. & Sills E. (2009) Economic impacts of invasive species in forests past, present, and future. Annals of the New York Academy of Sciences 1162, 1838.
Jennings D.E., Gould J.R., Vandenberg J.D., Duan J.J. & Shrewsbury P.M. (2013) Quantifying the impact of woodpecker predation on population dynamics of the emerald ash borer (Agrilus planipennis). PLoS ONE 8, e83491.
Jennings D.E., Taylor P.B. & Duan J.J. (2014) The mating and oviposition behavior of the invasive emerald ash borer (Agrilus planipennis), with reference to the influence of host tree condition. Journal of Pest Science 87, 7178.
Klooster W.S., Herms D.A., Knight K.S., Herms C.P., McCullough D.G., Smith A., Gandhi K.J.K. & Cardina J. (2014) Ash (Fraxinus spp.) mortality, regeneration, and seed bank dynamics in mixed hardwood forests following invasion by emerald ash borer (Agrilus planipennis). Biological Invasions 16, 859873.
Koenig W.D., Liebhold A.M., Bonter D.N., Hochachka W.M. & Dickinson J.L. (2013) Effects of the emerald ash borer invasion on four species of birds. Biological Invasions 15, 20952103.
Kovacs K.F., Haight R.G., McCullough D.G., Mercader R.J., Siegert N.W. & Liebhold A.M. (2010) Cost of potential emerald ash borer damage in US communities, 2009–2019. Ecological Economics 69, 569578.
Liebhold A.M., Macdonald W.L., Bergdahl D. & Maestro V.C. (1995) Invasion by exotic forest pests: a threat to forest ecosystems. Forest Science 41, 149.
Limback C.K., McCullouch D.G., Chen Y.G., Poland T.M. & Cregg B.M. (2010) Host vigor and emerald ash borer larvae on green and white ash. pp. 4547 in Lance D., Buck J., Binion D., Mastro V. & Reardon R. (Eds) Proceedings of the Emerald Ash Borer Research and Technology Development Meeting, Pittsburgh, PA, 20–21 October 2009, Morgantown, West Virginia, USDA Forest Service.
Lindell C.A., McCullough D.G., Cappaert D., Apostolou N.M. & Roth M.B. (2008) Factors influencing woodpecker predation on emerald ash borer. American Midland Naturalist 159, 434444.
Liu H.P., Bauer L.S., Miller D.L., Zhao T.H., Gao R.T., Song L.W., Luan Q.S., Jin R.Z. & Gao C.Q. (2007) Seasonal abundance of Agrilus planipennis (Coleoptera: Buprestidae) and its natural enemies Oobius agrili (Hymenoptera: Encyrtidae) and Tetrastichus planipennisi (Hymenoptera: Eulophidae) in China. Biological Control 42, 6171.
NOAA (2015) National Climatic Data Center. Available online at
Orlova-Bienkowskaja M.J. (2014) Ashes in Europe are in danger: the invasive range of Agrilus planipennis in European Russia is expanding. Biological Invasions 16, 13451349.
Poland T.M. & 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, 118124.
R Core Team (2014) R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing. Available online at
Rebek E.J., Herms D.A. & 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, 242246.
Rodriguez-Saona C.R., Miller J.R., Poland T.M., Kuhn T.M., Otis G.W., Turk T. & Ward D.L. (2007) Behaviors of adult Agrilus planipennis (Coleoptera: Buprestidae). Great Lakes Entomologist 40, 116.
Siegert N.W., McCullough D.G., Liebhold A.M. & Telewski F.W. (2014) Dendrochronological reconstruction of the epicentre and early spread of emerald ash borer in North America. Diversity and Distributions 20, 847858.
Smith A. (2006) Effects of community structure on forest susceptibility and response to the emerald ash borer invasion of the Huron River watershed in southeast Michigan. MS thesis, Ohio State University.
Sokal R.R. & Rohlf F.J. (1995) Biometry. New York, W. H. Reeman and Company.
Southwood R. & Henderson P.A. (2000) Ecological Methods. 3rd edn. Oxford, Blackwell Science.
Straw N.A., Williams D.T., Kulinich O. & Gninenko Y.I. (2013) Distribution, impact and rate of spread of emerald ash borer Agrilus planipennis (Coleoptera: Buprestidae) in the Moscow region of Russia. Forestry 86, 515522.
Tluczek A.R., McCullough D.G. & 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, 357366.
Ulyshen M.D., Klooster W.S., Barrington W.T. & Herms D.A. (2011) Impacts of emerald ash borer-induced tree mortality on leaf litter arthropods and exotic earthworms. Pedobiologia 54, 261265.
Wang X-Y., Yang Z-Q., Gould J.R., Zhang Y-N., Liu G-J. & Liu E-S. (2010) The biology and ecology of the emerald ash borer, Agrilus planipennis, in China. Journal of Insect Science 10, 128.
Warton D.I. & Hui F.K.C. (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92, 310.
Wei X., Wu Y., Reardon R., Sun T.H., Lu M. & Sun J.H. (2007) Biology and damage traits of emerald ash borer (Agrilus planipennis Fairmaire) in China. Insect Science 14, 367373.
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