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Natural enemies of emerald ash borer (Coleoptera: Buprestidae) in northeast China, with notes on two species of parasitic Coleoptera

Published online by Cambridge University Press:  07 December 2015

Xiao-Yi Wang ,
Liang-Ming Cao ,
Zhong-Qi Yang ,
Jian J. Duan ,
Juli R. Gould  and
Leah S. Bauer
Xiao-Yi Wang*
Affiliation:
Key Laboratory of Forest Protection, State Forestry Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing 100091, China
Liang-Ming Cao
Affiliation:
Key Laboratory of Forest Protection, State Forestry Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing 100091, China
Zhong-Qi Yang
Affiliation:
Key Laboratory of Forest Protection, State Forestry Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing 100091, China
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
Leah S. Bauer
Affiliation:
United States Department of Agriculture, Forest Service, Northern Research Station, Lansing, Michigan 48910, United States of America
*
1Corresponding author (e-mail: xywang@caf.ac.cn).
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Abstract

To investigate natural enemies of emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), in northeastern China, we conducted field surveys of ash (Fraxinus Linnaeus (Oleaceae)) trees in semi-natural forests and plantations at variable EAB densities from 2008 to 2013. Our surveys revealed a complex of natural enemies including eight hymenopteran parasitoids and two apparently parasitic Coleoptera, woodpeckers, and several undetermined mortality factors. Parasitoid complex abundance and its contribution to EAB mortality varied with the time of year, type of ash stands, and geographic regions. The egg parasitoid Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae) and the larval parasitoid Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae) were frequently observed in Jilin, Liaoning, and Heilongjiang provinces and in Beijing, but not in Tianjin. Spathius agrili Yang (Hymenoptera: Braconidae), however, was more prevalent near Beijing and further south in Tianjin. Larvae of two species of apparently parasitic beetle, Tenerus Laporte (Coleoptera: Cleridae) species and Xenoglena quadrisignata Mannerheim (Coleoptera: Trogossitidae), were also recovered attacking overwintering EAB in Liaoning Province, with Tenerus species being a dominant mortality agent (~13%). Our findings support the need to consider the geographic origin of insect natural enemies for EAB biocontrol, as well as an expanded foreign exploration for EAB natural enemies throughout its native range in Asia.

Type
Insect Management
Information
The Canadian Entomologist , Volume 148 , Issue 3 , June 2016 , pp. 329 - 342
Copyright
© Entomological Society of Canada 2015 

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Footnotes

Subject editor: Dylan Parry

References

Abell, K.J., Bauer, L.S., Duan, J.J., and Van Driesche, R.G. 2014. Impact of the introduced egg parasitoid, Oobius agrili (Hymenoptera: Encyrtidae), on emerald ash borer (Coleoptera: Buprestidae) in Michigan, USA. Biological Control, 79: 36–42.CrossRefGoogle Scholar
Bauer, L.S., Duan, J.J., and Gould, J.R. 2014. Emerald ash borer (Agrilus planipennis Fairmaire) (Coleoptera: Buprestidae). In The use of classical biological control to preserve forests in North America. Edited by R.G. Van Driesche and R. Reardon. FHTET-2013-02. United States Department of Agriculture, Forest Service, Forest Health Technology Enterprise Team, Morgantown, West Virginia, United States of America. Pp. 189–209.Google Scholar
Bauer, L.S., Duan, J.J., Gould, J.R., and Van Driesche, R.G. 2015. Progress in the classical biological control of Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) in North America. The Canadian Entomologist, 147: 300–317.Google Scholar
Bauer, L.S., Liu, H.P., Miller, D.L., and Gould, J.R. 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.Google Scholar
Belokobylskij, S.A., Yurchenko, G.I., Strazanac, J.S., Zaldívar-Riverón, A., and Mastro, V.A. 2012. 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.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. and McCullough, D.G. 2010. Phenology of Atanycolus cappaerti (Hymenoptera: Braconidae), a native parasitoid of emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae). Great Lakes Entomologist, 41: 141–154.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: 152–163.CrossRefGoogle Scholar
Clausen, C.P. 1940. Entomophagous insects. McGraw-Hill Book Company, New York, New York, United States of America. Pp. 545–548.Google Scholar
Duan, J.J., Abell, K.J., Bauer, L.S., and Van Driesche, R.G. 2014. Natural enemies implicated in the regulations of an invasive pest: a life table analysis of the population dynamics of the invasive emerald ash borer. Agricultural and Forest Entomology, 16: 406–416.Google Scholar
Duan, J.J., Bauer, L.S., Abell, K., Lelito, J., and Van Driesche, R.G. 2013. 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.G. 2012a. 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.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.Google 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., Taylor, P.B., and Fuester, R.W. 2011. Biology and life history of Balcha indica, an ectoparasitoid attacking the emerald ash borer, Agrilus planipennis, in North America. Journal of Insect Science (Madison), 11: 127.Google ScholarPubMed
Duan, J.J., Ulyshen, M.D., Bauer, L.S., Gould, J.R., and Van Driesche, R.G. 2010. Measuring the impact of biotic factors on populations of immature emerald ash borer (Coleoptera: Buprestidae). Environmental Entomology, 39: 1513–1522.Google Scholar
Duan, J.J., Yurchenko, G., and Fuester, R.W. 2012c. Occurrence of emerald ash borer (Coleoptera: Buprestidae) and biotic factors affecting its immature stages in the Russian Far East. Environmental Entomology, 41: 245–254.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.Google Scholar
Haack, R.A., Jendek, E., Liu, H.P., 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
Herms, D.A. 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.Google Scholar
Jennings, D.E., Gould, J.R., Vandenberg, J.D., Duan, J.J., and Shrewsbury, P.M. 2013. Quantifying the effects of woodpecker predation on population dynamics of the emerald ash borer (Agrilus planipennis). Public Library of Science One, 8: e83491, doi:10.1371/journal.pone.0083491.Google Scholar
Kim, J. and Jung, B.H. 2006. Taxonomic review of the Cleridae (Coleoptera) in Korea (part 2): Enopliinae Gistel, 1856. Entomological Research, 36: 20–23.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. The American Midland Naturalist, 159: 434–444.Google Scholar
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. Great Lakes Entomologist, 36: 191–204.Google Scholar
Liu, H.P., Bauer, L.S., Miller, D.L., Zhao, T.H., Gao, R.T., Song, L.W., 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.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. Great Lakes Entomologist, 42: 8–15.Google Scholar
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: 1345–1349.Google 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
SAS Institute Inc. 2012. JMP Pro 10.0.1 Introductory guide. SAS Institute Inc., Cary, North Carolina, United States of America.Google Scholar
Taylor, P.B., Duan, J.J., Fuester, R.W., Hoddle, M., and Van Driesche, R.G. 2012. Parasitoid guilds of Agrilus woodborers (Coleoptera: Buprestidae): their diversity and potential for use in biological control. Psyche, 813929: 1–10.Google Scholar
Van Driesche, R.G. 2014. Biological control of forest pests in North America: a reflection. In The use of classical biological control to preserve forests in North America. Edited by R.G. Van Driesche and R. Reardon. FHTET-2013-02. United States Department of Agriculture, Forest Service, Forest Health Technology Enterprise Team, Morgantown, West Virginia, United States of America. Pp. 1–8.Google Scholar
Van Driesche, R.G., Hoddle, M., and Center, T. 2008. Control of pests and weeds by natural enemies: an introduction to biological control. Blackwell, Malden, Massachusetts, United States of America.Google 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: 128.Google Scholar
Wei, J.R., Yang, Z.Q., Poland, T.M., and Du, J.W. 2009. Parasitism and olfactory responses of Dastarcus helophoroides (Coleoptera: Bothrideridae) to different cerambycid hosts. BioControl, 54: 733–742.CrossRefGoogle Scholar
Wei, X., Wu, Y., Reardon, R.D., 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.Google Scholar
Yang, Z.Q., Strazanac, J.S., Marsh, P.M., van Achterberg, C., and Choui, W.Y. 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.Google Scholar
Yang, Z.Q., Strazanac, J.S., Yao, Y.X., and Wang, X.Y. 2006. A new species of emerald ash borer parasitoid from China belonging to the genus Tetrastichus Haliday (Hymenoptera: Eulophidae). Proceedings of the Entomological Society of Washington, 108: 550–558.Google 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
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, 33: 253–260.Google Scholar