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Progress in the classical biological control of Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) in North America

Published online by Cambridge University Press:  12 May 2015

Leah S. Bauer ,
Jian J. Duan ,
Juli R. Gould  and
Roy Van Driesche
Leah S. Bauer*
Affiliation:
United States Department of Agriculture, Forest Service, Northern Research Station, Lansing, Michigan 48910, United States of America
Jian J. Duan
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Beneficial Insects Introduction Research Unit, Newark, Delaware 19713, United States of America
Juli R. Gould
Affiliation:
United States Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine, Center for Plant Health Science and Technology, Buzzards Bay, Massachusetts 02542, United States of America
Roy Van Driesche
Affiliation:
Department of Environmental Conservation, University of Massachusetts, Amherst, Massachusetts 01003, United States of America
*
1Corresponding author (e-mail: lbauer@fs.fed.us)
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Abstract

First detected in North America in 2002, the emerald ash borer (EAB) (Agrilus planipennis Fairmaire; Coleoptera: Buprestidae), an invasive phloem-feeding beetle from Asia, has killed tens of millions of ash (Fraxinus Linnaeus; Oleaceae) trees. Although few parasitoids attack EAB in North America, three parasitoid species were found attacking EAB in China: the egg parasitoid Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae) and two larval parasitoids Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae) and Spathius agrili Yang (Hymenoptera: Braconidae). In 2007, classical biological control of EAB began in the United States of America after release of these three species was approved. In 2013, release of the larval parasitoids was approved in Canada. Research continues at study sites in Michigan, United States of America where the establishment, prevalence, and spread of O. agrili and T. planipennisi have been monitored since 2008. However, establishment of S. agrili remains unconfirmed in northern areas, and its release is now restricted to regions below the 40th parallel. In 2015, approval for release of Spathius galinae Belokobylskij (Hymenoptera: Braconidae), an EAB larval parasitoid from the Russian Far East, may be granted in the United States of America. Researchers are guardedly optimistic that a complex of introduced and native natural enemies will regulate EAB densities below a tolerance threshold for survival of ash species or genotypes in forested ecosystems.

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Type
Original Article
Information
The Canadian Entomologist , Volume 147 , Special Issue 3: Emerald Ash Borer , June 2015 , pp. 300 - 317
Copyright
© Entomological Society of Canada 2015. This is a work of the U.S. Government and is not subject to copyright protection in the United States. 

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Footnotes

Subject editor: Krista Ryall

References

Abell, K.J., Bauer, L.S., Duan, J.J., and Van Driesche, R.G. 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: 36–42.CrossRefGoogle Scholar
Abell, K.J., Duan, J.J., Bauer, L.S., Lelito, J.P., and Van Driesche, R.G. 2012. The effect of bark thickness on the effectiveness of Tetrastichus planipennisi (Hymen: Eulophidae) and Atanycolus spp. (Hymen: Braconidae) two parasitoids of emerald ash borer (Coleop: Buprestidae). Biological Control, 63: 320–325.CrossRefGoogle Scholar
Akiyama, K. and Ohmomo, S. 1997. A checklist of the Japanese Buprestidae. Gekkan-Mushi Supplement, 1: 1–67.Google 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
Badendreier, D., Bilger, F., and Kuhlmann, U. 2005. Methods to assess non-target effects of invertebrate biological control agents of arthropod pests. Biological Control, 50: 821–870.Google Scholar
Barter, G.W. 1957. Studies of the bronze birch borer, Agrilus anxius Gory, in New Brunswick. The Canadian Entomologist, 89: 12–36.CrossRefGoogle 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., Duan, J.J., and Gould, J. 2014. Emerald ash borer (Agrilus planipennis Fairmaire) (Coleoptera: Buprestidae). In The use of classical biological control to preserve forests in North America. FHTET-2013-02. Edited by R. Van Driesche and R. Reardon. United States Department of Agriculture, Forest Service, Forest Health Technology Enterprise Team, Morgantown, West Virginia, United States of America. Pp. 189–209. Available from http://www.fs.fed.us/foresthealth/technology/pdfs/FHTET-2013-2.pdf [accessed 11 March 2015].Google Scholar
Bauer, L.S., Duan, J.J., Lelito, J.P., Liu, H.P., and Gould, J.R. 2015. Biology of emerald ash borer parasitoids. In The biology and control of emerald ash borer. FHTET-2014-09. Edited by R.G. Van Driesche and R. Reardon. United States Department of Agriculture, Forest Service, Morgantown, West Virginia, United States of America. Pp. 97–112.Google Scholar
Bauer, L.S., Liu, H.P., Haack, R.A., Miller, D.L., and Petrice, T.R. 2004. Natural enemies of emerald ash borer in southeastern Michigan. In Proceedings of the emerald ash borer research and technology meeting, Port Huron, Michigan. 30 September–1 October 2003, FHTET-2004-02. Compiled by V. Mastro and R. Reardon. United States Department of Agriculture, Forest Service, Morgantown, West Virginia, United States of America. Pp. 33–34. Available from http://www.nrs.fs.fed.us/pubs/jrnl/2003/nc_2003_bauer_004.pdf [accessed 11 August 2014].Google Scholar
Bauer, L.S., Liu, H.P., Miller, D.L., and Gould, J. 2008. Developing a classical biological control program for Agrilus planipennis (Coleoptera: Buprestidae), an invasive ash pest in North America. Newsletter of the Michigan Entomological Society, 53: 38–39. Available from http://www.nrs.fs.fed.us/pubs/1439 [accessed 11 August 2014].Google Scholar
Belokobylskij, S.A., Yurchenko, G.I., Zaldívar-Riverón, A., Strazanac, J., and Mastro, V. 2012. A new emerald ash borer (Coleoptera: Buprestidae) parasitoid species of Spathius Nees (Hymenoptera: Braconidae: Doryctinae) from the Russian Far East and South Korea. Annals of the Entomological Society of America, 105: 165–178.CrossRefGoogle Scholar
Bray, A.M., Bauer, L.S., Poland, T.M., Haack, R.A., Cognato, A.I., and Smith, J.J. 2011. Genetic analysis of emerald ash borer (Agrilus planipennis Fairmaire) populations in Asia and North America. Biological Invasions, 13: 2869–2887.CrossRefGoogle Scholar
Canadian Food Inspection Agency. 2014. Agrilus planipennis – emerald ash borer [online]. Available from http://www.inspection.gc.ca/plants/plant-protection/insects/emerald-ash-borer/eng/1337273882117/1337273975030 [accessed 11 March 2015].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). The 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
Castrillo, L.A., Bauer, L.S., Houping, L.P., 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
Chinese Academy of Science, Institute of Zoology. 1986. Agrilus marcopoli Obenberger. Agriculture Insects of China (Part I). China Agriculture Press, Beijing, China. P. 445. Available from http://www.nrs.fs.fed.us/disturbance/invasive_species/eab/local-resources/downloads/biologyCAS1986.pdf [accessed 5 September 2014].Google Scholar
Côté, W.A. and Allen, D.C. 1980. Biology of two-lined chestnut borer, Agrilus bilineatus, in Pennsylvania and New York (Coleoptera: Buprestidae). Annals of the Entomological Society of America, 73: 409–413.CrossRefGoogle Scholar
Duan, J.J., Abell, K.J., Bauer, L.S., Gould, J., and Van Driesche, R.A. 2014a. 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: 406–416.CrossRefGoogle Scholar
Duan, J.J., Bauer, L.S., Abell, K.J., Lelito, J.P., and Van Driesche, R. 2013a. 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: 1145–1154.CrossRefGoogle ScholarPubMed
Duan, J.J., Bauer, L.S., Abell, K.J., and Van Driesche, R. 2012a. Population responses of hymenopteran parasitoids to the emerald ash borer (Coleoptera: Buprestidae) in recently invaded areas in north central United States. Biological Control, 57: 199–209.Google Scholar
Duan, J.J., Bauer, L.S., Hansen, J.A., Abell, K.J., and Van Driesche, R. 2012b. 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: 255–261.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 emerald ash borer (Coleoptera: Buprestidae). Biological Control, 56: 170–174.CrossRefGoogle Scholar
Duan, J.J., Fuester, R.W., Wildonger, J., Taylor, P.H., 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., Oppel, C.B., Ulyshen, M.D., Bauer, L.S., and Lelito, J. 2011b. Biology and life history of Tetrastichus planipennisi (Hymenoptera: Eulophidae), a larval endoparasitoid of the emerald ash borer. Florida Entomologist, 94: 933–940.CrossRefGoogle Scholar
Duan, J.J., Taylor, P.B., and Fuester, R.W. 2011c. Biology and life history of Balcha indica, an ectoparasitoid attacking the emerald ash borer, Agrilus planipennis, in North America. Journal of Insect Science, 11: 1–9. Available from http://jinsectscience.oxfordjournals.org/content/jis/11/1/127.full.pdf [accessed 11 March 2015].CrossRefGoogle ScholarPubMed
Duan, J.J., Taylor, P.H., 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, 39: 1513–1522.CrossRefGoogle ScholarPubMed
Duan, J.J., Watt, T.J., and Larson, K. 2014b. Biology, life history, and laboratory rearing of Spathius galinae (Hymenoptera: Braconidae), a larval parasitoid of the invasive emerald ash borer (Coleoptera: Buprestidae). Journal of Economic Entomology, 107: 939–946.CrossRefGoogle ScholarPubMed
Duan, J.J., Watt, T., Taylor, P., Larson, K., and Lelito, J.P. 2013c. 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: 2101–2108.CrossRefGoogle ScholarPubMed
Duan, J.J., Yurchenko, G., and Fuester, R. 2012c. Occurrence of emerald ash borer (Coleoptera: Buprestidae) and biotic factors affecting its immature stages in far eastern Russia. Environmental Entomology, 41: 245–254.CrossRefGoogle Scholar
Federal Register. 2003. Emerald ash borer: quarantine and regulations. 7 CFR Part 301 [docket Number 02-125-1]. Available from https://www.federalregister.gov/articles/2003/10/14/03-25881/emerald-ash-borer-quarantine-and-regulations [accessed 9 October 2014].Google Scholar
Federal Register. 2007. Availability of an environmental assessment for the proposed release of three parasitoids for the biological control of the emerald ash borer (Agrilus planipennis) in the continental United States. Federal Register, 72: 28947–28948. [docket number APHIS-2007-006]. Available from http://www.regulations.gov/#!documentDetail;D=APHIS-2007-0060-0043 [accessed 9 October 2014].Google Scholar
Federal Register. 2015. Field release of the parasitoid Spathius galinae for the biological control of the emerald ash borer (Agrilus planipennis) in the continental United States. Federal Register, 80: 7827 [docket number APHIS-2014-0094]. Available from http://www.regulations.gov/#!docketDetail;D=APHIS-2014-0094 [accessed 19 February 2015].Google 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
Gould, J., Ayer, T., and Fraser, I. 2011. Effects of rearing conditions on reproduction of Spathius agrili (Hymenoptera: Braconidae), a parasitoid of the emerald ash borer (Coleoptera: Buprestidae). Journal of Economic Entomology, 104: 379–387.CrossRefGoogle ScholarPubMed
Gould, J., Fraser, I., Yang, Z., Wang, X., Mastro, V., and Williams, D. 2009. Update on EAB biocontrol: release and recovery of Spathius agrili and discovery of new potential biocontrol agents in Asia. In Proceedings of the 20th USDA Interagency Research Forum on Invasive Species 2009. Annapolis, MD 13–16 January 2009, General Technical Report NRS-P-51. Edited by K. McManus and K. Gottschalk, United States Department of Agriculture, Forest Service, Newtown Square, Pennsylvania, United States of America. P. 29. Available from http://nrs.fs.fed.us/pubs/34230 [accessed 11 August 2014].Google Scholar
Government Accounting Office. 2006. Invasive forest pests: lessons learned from three recent infestations may aid in managing future efforts. Report of the United States Government Accounting Office, GAO-06–353. Available from http://www.gao.gov/assets/250/249776.pdf [accessed 9 October 2014].Google 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 twolined chestnut borer, Agrilus bilineatus (Coleoptera: Buprestidae), in Wisconsin. The Great Lakes Entomologist, 14: 113–116.Google Scholar
Haack, R.A., Jendek, E., Liu, H.P., Marchant, K., Petrice, T., Poland, T., et al. 2002. The emerald ash borer: a new exotic pest in North America. Newsletter of the Michigan Entomological Society, 47: 1–5. Available from http://nrs.fs.fed.us/pubs/jrnl/2002/nc_2002_Haack_001.pdf [accessed 11 August 2014].Google Scholar
Hanson, A.A., Venette, R.C., and Lelito, J.P. 2013. Cold tolerance of Chinese emerald ash borer parasitoids: Spathius agrili Yang (Hymenoptera: Braconidae), Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae), and Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae). Biological Control, 67: 516–529.CrossRefGoogle Scholar
Herms, D.A. and McCullough, D.G. 2014. Emerald ash borer invasion of North America: history, biology, ecology, impact and management. Annual Review of Entomology, 59: 13–30.CrossRefGoogle Scholar
Jendek, E. 1994. Studies in the east Palaearctic species of the genus Agrilus Dahl, 1823 (Coleoptera: Buprestidae). Part I. Entomological Problems, 25: 9–25.Google Scholar
Jendek, E. and Grebennikov, V.V. 2011. Agrilus (Coleoptera, Buprestidae) of east Asia. Jan Farkac, Prague, Czech Republic.Google Scholar
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) [online]. Public Library of Science One, 8: e83491. doi:10.1371/journal.pone.0083491.Google Scholar
Johnson, T.D., Lelito, J.P., and Raffa, K.F. 2014. Responses of two parasitoids, the exotic Spathius agrili Yang and the native Spathius floridanus Ashmead, to volatile cues associated with the emerald ash borer, Agrilus planipennis Fairmaire. Biological Control, 79: 110–117.CrossRefGoogle Scholar
Kashian, D.M., Bauer, L.S., and Spei, B.A. In press. Potential impacts of emerald ash borer biocontrol on ash health and recovery in southern Michigan. In Proceedings of the emerald ash borer research and technology development meeting, Wooster, Ohio, 15–16 October 2014. FHTET-2015. Compiled by D. Lance and R. Reardon. United States Department of Agriculture, Forest Service, Morgantown, West Virginia, United States of America.Google Scholar
Keever, C.C., Nieman, C., Ramsay, L., Ritland, C.E., Bauer, L.S., Lyons, D.B., et al. 2013. Microsatellite population genetics of the emerald ash borer (Agrilus planipennis Fairmaire): comparisons between Asian and North American populations suggest multiple introductions. Biological Invasions, 15: 1537–1559.CrossRefGoogle Scholar
Ko, J.H. 1969. A list of forest insect pests in Korea. Forest Research Institute, Seoul, South Korea.Google Scholar
Koenig, W.D., Liebhold, A., 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
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
Kula, R.R., Knight, K.S., Rebbeck, J., Cappaert, D., Bauer, L.S., 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
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.P. and Bauer, L.S. 2006. Susceptibility of Agrilus planipennis (Coleoptera: Buprestidae) to Beauveria bassiana and Metarhizium anisopliae. Journal of Economic Entomology, 99: 1096–1103.CrossRefGoogle ScholarPubMed
Liu, H.P., Bauer, L.S., Gao, R.T., Zhao, T.H., 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. The Great Lakes Entomologist, 36: 191–204. Available from http://nrs.fs.fed.us/pubs/jrnl/2003/nc_2003_liu_001.pdf [accessed 11 August 2014].Google Scholar
Liu, H.P., Bauer, L.S., Miller, D.L., Zhao, T.H., Gao, R.T., Song, L., et al. 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: 61–71.CrossRefGoogle Scholar
Liu, H.Q., Ma, R.S., and Li, Q.H. 1996. Survey and management of emerald ash borer, Agrilus marcopoli. Agri-Forestry Science and Technology of Tianjin, 1: 46–48.Google Scholar
Loerch, C.R. and Cameron, E.A. 1983. Natural enemies of immature stages of the bronze birch borer, Agrilus anxius (Coleoptera: Buprestidae), in Pennsylvania. Environmental Entomology, 12: 1798–1801.CrossRefGoogle Scholar
MapBioControl 2014. Agent release tracking and data management for federal, state, and researchers releasing three biocontrol agents released against emerald ash borer. Available from http://www.mapbiocontrol.org [accessed 11 August 2014].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. The Great Lakes Entomologist, 42: 8–15.Google Scholar
McCullough, D.G. and Mercader, R.J. 2012. Evaluation of potential strategies to SLow Ash Mortality (SLAM) caused by emerald ash borer (Agrilus planipennis): SLAM in an urban forest. International Journal of Pest Management, 58: 9–23.CrossRefGoogle Scholar
Orlova-Bienkowskaja, M.J. and Belokobylskij, S.A. 2014. Discovery of the first European parasitoid of the emerald ash borer Agrilus planipennis (Coleoptera: Buprestidae). European Journal of Entomology, 111: 594–596.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
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
Roscoe, L.E. 2014. Phasgonophora sulcata Westwood (Hymenoptera: Chalcididae): a potential augmentative biological control agent for the invasive Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) in Canada. Ph.D. Dissertation. University of Toronto, Toronto, Ontario, Canada.Google 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: 847–858.CrossRefGoogle Scholar
Tang, Y.L., Wang, X.Y., Yang, Z.Q., Jiang, J., Wang, X.H., and Lu, J. 2012. Alternative hosts of Sclerodermus pupariae (Hymenoptera: Bethylidae), a larval parasitoid of the longhorn beetle Massicus raddei (Coleoptera: Cerambycidae). Acta Entomologica Sinica, 55: 55–62.Google Scholar
Taylor, P.B., Duan, J.J., Fuester, R.W., Hoddle, M., and Van Driesche, R. 2012. Parasitoid guilds of Agrilus woodborers (Coleoptera: Buprestidae): their diversity and potential for use in biological control. Psyche, 813929: 1–10. Available from http://www.hindawi.com/journals/psyche/2012/813929/ [accessed 9 October 2014].Google Scholar
Taylor, R.A.J., Bauer, L.S., Poland, T.M., and Windell, K. 2010. Flight performance of Agrilus planipennis (Coleoptera: Buprestidae) on a flight mill and in free flight. Journal of Insect Behavior, 23: 128–148.CrossRefGoogle Scholar
Tluczek, A.R., Cappaert, D., and McCullough, D.G. 2010. Life cycle of Atanycolus sp. nr. hicoriae, a newly described native parasitoid of emerald ash borer. In Proceedings of the emerald ash borer research and technology meeting, Pittsburgh, Pennsylvania, 20–21 October 2009. FHTET-2010-1. Compiled by D. Lance, R. Reardon, and V. Mastro. United States Department of Agriculture, Forest Service, Morgantown, West Virginia, United States of America. Pp. 91–92. Available from http://www.fs.fed.us/foresthealth/technology/pdfs/2009EAB.pdf [accessed 11 August 2014].Google Scholar
Ulyshen, M.D., Duan, J.J., and Bauer, L.S. 2010a. Suitability and accessibility of immature Agrilus planipennis (Coleoptera: Buprestidae) stages to Tetrastichus planipennisi (Hymenoptera: Eulophidae). Journal of Economic Entomology, 103: 1080–1085.CrossRefGoogle ScholarPubMed
Ulyshen, M.D., Duan, J.J., and Bauer, L.S. 2010b. Interactions between Spathius agrili (Hymenoptera: Braconidae) and Tetrastichus planipennisi (Hymenoptera: Eulophidae), larval parasitoids of Agrilus planipennis (Coleoptera: Buprestidae). Biological Control, 52: 188–193.CrossRefGoogle Scholar
United States Department of Agriculture. 2009. Emerald ash borer biological control program 5-year implementation strategy. October 2009. Available from http://www.nrs.fs.fed.us/disturbance/invasive_species/eab/local-resources/downloads/eab-biocontrol-5 yr-strategy_plan.pdf [accessed 11 August 2014].Google Scholar
United States Department of Agriculture. 2013. Emerald ash borer biological control release and recovery guidelines. United States Department of Agriculture, Animal and Plant Health Inspection Service, Forest Service, Agricultural Research Service, Riverdale, Maryland, United States of America. Available from http://www.aphis.usda.gov/plant_health/plant_pest_info/emerald_ash_b/downloads/EAB-FieldRelease-Guidelines.pdf [accessed 11 August 2014].Google Scholar
United States Department of Agriculture, Animal and Plant Health Inspection Service (APHIS). 2014. Emerald ash borer program manual, ver. 1.3, revised July 2013 [online]. Available from http://www.aphis.usda.gov/import_export/plants/manuals/domestic/downloads/emerald_ash_borer_manual.pdf [accessed 11 August 2014].Google Scholar
Wang, X.Y., Yang, Z.Q., Gould, J.R., Wu, H., and Ma, J.H. 2010. Host-seeking behavior and parasitism by Spathius agrili Yang (Hymenoptera: Braconidae), a parasitoid of the emerald ash borer. Biological Control, 52: 24–29.CrossRefGoogle Scholar
Wang, X.Y., Yang, Z.Q., Liu, G.J., and Liu, E.S. 2006. Relationships between the emergence and oviposition of ectoparasitoid Spathius agrili Yang and its host emerald ash borer, Agrilus planipennis Fairmaire. Acta Ecologica Sinica, 26: 1103–1109.Google Scholar
Wang, X.Y, Yang, Z.Q., Wu, H., and Gould, J.R. 2008. Effects of host size on the sex ratio, clutch size, and size of adult Spathius agrili, an ectoparasitoid of emerald ash borer. Biological Control, 44: 7–12.CrossRefGoogle Scholar
Williams, D., Lee, H.P., and Jo, Y.S. 2005. Exploration for natural enemies of emerald ash borer in South Korea during 2004. In Proceedings of the emerald ash borer research and technology meeting, Romulus, Michigan, 5–6 October 2004. FHTET-2004-15. Compiled by V. Mastro and R. Reardon. United States Department of Agriculture, Forest Service, Morgantown, West Virginia, United States of America. P. 66, Available from http://www.fs.fed.us/foresthealth/technology/pdfs/2004EAB.pdf [accessed 11 August 2014].Google Scholar
Williams, D., Lee, H.P., and Jo, Y.S. 2006. Exploration for emerald ash borer and its natural enemies in South Korea during May–June 2005. In Proceedings of the emerald ash borer research and technology meeting, Pittsburgh, Pennsylvania, 26–27 September 2005. FHTET-2005-16. Compiled by V. Mastro and R. Reardon. United States Department of Agriculture, Forest Service, Morgantown, West Virginia, United States of America. P. 52. Available from http://www.fs.fed.us/foresthealth/technology/pdfs/2005EAB.pdf [accessed 11 August 2014].Google Scholar
Williams, D., Lee, H.P., Jo, Y.S., Yurchenko, G.I., and Mastro, V.C. 2010. Exploration for emerald ash borer and its natural enemies in South Korea and the Russian Far East 2004–2009. In Proceedings of the emerald ash borer research and technology meeting, Pittsburgh, Pennsylvania, 20–21 October 2009. FHTET-2010-1. Compiled by D. Lance, R. Reardon, and V. Mastro. United States Department of Agriculture, Forest Service, Morgantown, West Virginia, United States of America. Pp. 93–94. Available from http://www.fs.fed.us/foresthealth/technology/pdfs/2009EAB.pdf [accessed 11 August 2014].Google Scholar
Wu, H., Wang, X.Y., Li, M.L., Yang, Z.Q., Zeng, F.X., Wang, H.Y., et al. 2008. Biology and mass rearing of Sclerodermus pupariae Yang et Yao (Hymenoptera: Bethylidae), an important ectoparasitoid of the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae) in China. Acta Entomologica Sinica, 51: 46–54.Google Scholar
Xu, G.T. 2003. Agrilus marcopoli Obenberger. In Atlas of ornamental pests and diseases. Edited by G.T. Xu. China Agriculture Press, Beijing, China. Pp. 321–322.Google Scholar
Yang, Z.Q., Achterberg, C.V., Choi, W.Y., and Marsh, P.M. 2005. First recorded parasitoid from China of Agrilus planipennis: a new species of Spathius (Hymenoptera: Braconidae: Doryctinae). Annals of the Entomological Society of America, 98: 636–642.CrossRefGoogle Scholar
Yang, Z.Q., Wang, X.Y., Gould, J.R., and Wu, H. 2008. Host specificity of Spathius agrili Yang (Hymenoptera: Braconidae), an important parasitoid of the emerald ash borer. Biological Control, 47: 216–221.CrossRefGoogle Scholar
Yang, Z.Q., Wang, X.Y., Yao, Y.X., Gould, J.R., and Cao, L.M. 2012. A new species of Sclerodermus (Hymenoptera: Bethylidae) parasitizing Agrilus planipennis (Coleoptera: Buprestidae) from China, with a key to Chinese species in the genus. Annals of the Entomological Society of America, 105: 619–627.CrossRefGoogle Scholar
Yang, Z.Q., Yao, Y.X., and Wang, X.Y. 2006. A new species of emerald ash borer parasitoid from China belonging to the genus Tetrastichus (Hymneoptera: Eulophidae). Proceedings of the Entomological Society of Washington, 108: 550–558.Google Scholar
Yu, C. 1992. Agrilus marcopoli Obenberger. In Forest insects China, 2nd edition. Edited by G. Xiao. China Forestry Publishing House, Beijing, China. Pp. 400–401. Translation available from http://www.nrs.fs.fed.us/disturbance/invasive_species/eab/local-resources/downloads/biologyYu1992.pdf [accessed 11 August 2014].Google Scholar
Zhang, L.Y., Chen, Z.X., Yang, G.D., Huang, Q.Y., and Huang, Q.S. 1995. Control techniques for Agrilus marcopoli on velvet ash, Fraxinus velutina. Bulletin of Horticulture Science and Technology of Tianjin, 26: 1–7.Google Scholar
Zhang, Y.Z., Huang, D.W., Zhao, T.H., Liu, H.P., and Bauer, L.S. 2005. Two new species of egg parasitoids (Hymenoptera: Encyrtidae) of wood-boring beetle pests from China. Phytoparasitica, 53: 253–260.CrossRefGoogle Scholar
Zhao, T.H., Gao, R.T., Liu, H.P., Bauer, L.S., and Sun, L.Q. 2005. Host range of emerald ash borer, Agrilus planipennis Fairmaire, its damage and the countermeasures. Acta Entomologica Sinica, 48: 594–599.Google Scholar