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North American hymenopteran parasitoids of emerald ash borer larvae: seasonal abundance and interaction with introduced Asian parasitoids

Published online by Cambridge University Press:  10 February 2025

Toby R. Petrice Open the ORCID record for Toby R. Petrice [Opens in a new window] ,
Therese M. Poland Open the ORCID record for Therese M. Poland [Opens in a new window] ,
Leah S. Bauer ,
John S. Strazanac ,
Jian J. Duan ,
Jonathan M. Schmude  and
F. William Ravlin
Toby R. Petrice*
Affiliation:
United States Department of Agriculture Forest Service, Northern Research Station, East Lansing, Michigan, United States of America
Therese M. Poland
Affiliation:
United States Department of Agriculture Forest Service, Northern Research Station, East Lansing, Michigan, United States of America
Leah S. Bauer
Affiliation:
United States Department of Agriculture Forest Service, Northern Research Station, East Lansing, Michigan, United States of America
John S. Strazanac
Affiliation:
Department of Plant and Soil Sciences, West Virginia University, Ithaca, Michigan, United States of America
Jian J. Duan
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Beneficial Insects Introduction Research Unit, Newark, Delaware, United States of America
Jonathan M. Schmude
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Beneficial Insects Introduction Research Unit, Newark, Delaware, United States of America
F. William Ravlin
Affiliation:
Department of Entomology, Michigan State University, East Lansing, Michigan, United States of America
*
Corresponding author: Toby R. Petrice; Email: toby.petrice@usda.gov
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Abstract

In Michigan, United States of America, where Asian parasitoids were released to manage emerald ash borer, Agrilus planipennis Fairmaire (Coleoptera: Buprestidae), we monitored four native parasitoids that also attack the invasive beetle – Atanycolus cappaerti Marsh and Strazanac, A. simplex (Cresson), and Spathius laflammei Provancher (all Hymenoptera: Braconidae), and Phasgonophora sulcata Westwood (Hymenoptera: Chalcididae) – using yellow pan traps and tree dissections. Adult A. cappaerti, followed by A. simplex, had the broadest seasonal activity, S. laflammei was captured primarily in the first half of the growing season, and P. sulcata was restricted to mid-summer. Adult abundances of native species varied among years but, except for P. sulcata, were never significantly lower than the established Asian emerald ash borer larval parasitoids, Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae) and Spathius galinae Belokobylskij and Strazanac (Hymenoptera: Braconidae). Densities of emerald ash borer larvae parasitised by A. cappaerti or P. sulcata did not differ significantly from those of the two Asian species. Although adult A. simplex and S. laflammei were frequently captured, we did not confirm parasitisation of any emerald ash borer larvae by these two species, suggesting that they rarely attack emerald ash borer. We did not find any negative correlations between adult or immature parasitoid abundance of any parasitoid species, suggesting that any interspecific competition that may be occurring is negligible.

Type
Research Paper
Information
The Canadian Entomologist , Volume 157 , 2025 , e7
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Copyright
© The Author(s), 2025. Published by Cambridge University Press on behalf of Entomological Society of Canada

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Footnotes

*

Retired

Subject editor: Maya Evenden

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. https://doi.org/10.1016/j.biocontrol.2012.08.009.CrossRefGoogle Scholar
Bauer, L.S., Duan, J.J., Gould, J.R., and Van Driesche, R. 2015a. Progress in the classical biological control of Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) in North America. The Canadian Entomologist, 147: 300–317. https://doi.org/10.4039/tce.2015.18.CrossRefGoogle Scholar
Bauer, L.S., Duan, J.J., Lelito, J.P., Liu, H., Gould, J.R., Bauer, L.S., et al. 2015b. Biology of emerald ash borer parasitoids. In Biology and Control of Emerald Ash Borer. FHTET-2014-09. Edited by van Driesche, R.G. and Reardon, R.. United States Department of Agriculture, Forest Service, Forest Health Technology Enterprise Team, Morgantown, West Virginia, United States of America. Pp. 97–112. https://www.fs.usda.gov/nrs/pubs/jrnl/2015/nrs_2015_bauer_002.pdf [accessed 30 October 2024].Google Scholar
Belokobylskij, S.A., Yurchenko, G.I., Strazanac, J.S., Zaldívar-Riverón, A., 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. https://doi.org/10.1603/an11140.CrossRefGoogle Scholar
Butler, S., Dedes, J., Jones, G., Hughes, C., Ladd, T., Martel, V., et al. 2022. Introduction and establishment of biological control agents for control of emerald ash borer (Agrilus planipennis) in Canada. The Canadian Entomologist, 154: 1–20. https://doi.org/10.4039/tce.2022.32.CrossRefGoogle Scholar
Canadian Food Inspection Agency. 2024. Import and release of biological control agents into Canada. [Online.] Available from https://inspection.canada.ca/plant-health/invasive-species/biologicalcontrol-agents/eng/1514956211166/1514956212112 [accessed 27 August 2024].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
Duan, J.J., Bauer, L.S., Abell, K.J., Ulyshen, M.D., and Van Driesche, R.G. 2015. Population dynamics of an invasive forest insect and associated natural enemies in the aftermath of invasion: implications for biological control. Journal of Applied Ecology, 52: 1246–1254. https://doi.org/10.1111/1365-2664.12485.CrossRefGoogle Scholar
Duan, J.J., Bauer, L.S., van Driesche, R.G., and Gould, J.R. 2018. Progress and challenges of protecting North American ash trees from the emerald ash borer using biological control. Forests, 9: 1–17. https://doi.org/10.3390/f9030142.CrossRefGoogle Scholar
Duan, J., Fuester, R.W.F., Wildonger, J.W., Taylor, P.B., Barth, S.B., and Spichiger, S.E.S. 2009. Parasitoids attacking the emerald ash borer (Coleoptera: Buprestidae) in western Pennslyvania. Florida Entomologist, 92: 588–592. https://doi.org/10.1653/024.092.0409.Google Scholar
Duan, J.J., Gould, J.R., Quinn, N.F., Petrice, T.R., Slager, B.H., Poland, T.M., et al. 2023a. Protection of North American ash against emerald ash borer with biological control: ecological premises and progress toward success. BioControl, 68: 87–100. https://doi.org/10.1007/s10526-023-10182-w.CrossRefGoogle Scholar
Duan, J.J., Gould, J., Slager, B.H., Quinn, N.F., Petrice, T.R., Poland, T.M., et al. 2022. Progress toward successful biological control of the invasive emerald ash borer in the United States. In Contributions of Classical Biological Control to the U.S. Food Security, Forestry, and Biodiversity. FHAAST-2019-05. Edited by Van Driesche, R.G., Winston, R.L., Perring, T.M., and Lopez, V.M.. United States Department of Agriculture, Forest Service, Forest Health Technology Enterprise Team, Morgantown, West Virginia, United States of America. Pp. 232–250. Available from https://www.fs.usda.gov/foresthealth/technology/pdfs/FHAAST-2019-05-Contributions-Classical-Biocontrol.pdf [accessed 30 October 2024].Google Scholar
Duan, J.J. and Schmude, J. 2016. Biology and life history of Atanycolus cappaerti (Hymenoptera: Braconidae), a North American larval parasitoid attacking the invasive emerald ash borer (Coleoptera: Buprestidae). Florida Entomologist, 99: 722–728. https://doi.org/10.1653/024.099.0423.CrossRefGoogle Scholar
Duan, J.J., Schmude, J.M., Petrice, T.R., Bauer, L.S., Poland, T.M., Chandler, J.L., et al. 2023b. Successful establishment, spread, and impact of the introduced parasitoid Spathius galinae (Hymenoptera: Braconidae) on emerald ash borer (Coleoptera: Buprestidae) populations in postinvasion forests in Michigan. Journal of Economic Entomology, 116: 1518–1528. https://doi.org/10.1093/jee/toad149.CrossRefGoogle ScholarPubMed
Duan, J.J., Taylor, P.B., Fuester, R.W., Kula, R.R., and Marsh, P.M. 2013. Hymenopteran parasitoids attacking the invasive emerald ash borer (Coleoptera: Buprestidae) in western and central Pennsylvania. Florida Entomologist, 96: 166–172. https://doi.org/10.1653/024.096.0122.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. https://doi.org/10.1603/en10023.CrossRefGoogle ScholarPubMed
Duan, J.J., Van Driesche, R.G., Schmude, J.M., Quinn, N.F., Petrice, T.R., Rutledge, C.E., et al. 2021. Niche partitioning and coexistence of parasitoids of the same feeding guild introduced for biological control of an invasive forest pest. Biological Control, 160: 104698. https://doi.org/10.1016/j.biocontrol.2021.104698.CrossRefGoogle Scholar
Gaudon, J.M., Lyons, D.B., Jones, G.C., Allison, J.D., and Smith, S.M. 2020. Evaluating methods to detect and monitor North American larval parasitoids of the emerald ash borer (Coleoptera: Buprestidae). The Canadian Entomologist, 152: 389–398. https://doi.org/10.4039/tce.2020.8.CrossRefGoogle Scholar
Haack, R.A., Benjamin, D.M., and Schuh, B.A. 1981. Observations of the biology of Phasgonophora sulcata (Hymenoptera: Chalcididae), a larval parasitoid of the twolined chestnut borer, Agrilus bilineatus (Coleoptera: Buprestidae), in Wisconsin. Great Lakes Entomologist, 14: 113–116. https://doi.org/10.22543/0090-0222.1386.Google Scholar
Haack, R.A., Jendek, E., Liu, H., Marchant, K.R., Petrice, T.R., Poland, T.M., and Ye, H. 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. https://doi.org/10.1146/annurev-ento-011613-162051.CrossRefGoogle ScholarPubMed
Hooie, N.A., Wiggins, G.J., Lambdin, P.L., Grant, J.F., Powell, S.D., and Lelito, J.P. 2015. Native parasitoids and recovery of Spathius agrili from areas of release against emerald ash borer in eastern Tennessee, USA. Biocontrol Science and Technology, 25: 345–351. https://doi.org/10.1080/09583157.2014.971712.CrossRefGoogle Scholar
Krombein, K.V., Hurd, P.D. Jr., Smith, D.R., and Burks, B.D. 1979. Catalog of Hymenoptera in America North of Mexico. Volume 1. Smithsonian Institution Press, Washington, DC, United States of America.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
MapBioControl. 2024. Agent release tracking and data management for federal, state, and researchers releasing four biocontrol agents released against emerald ash borer. Available from http://www.mapbiocontrol.org/ [accessed 1 October 2019].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 Hymenopteran 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
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: 1577–1586. https://doi.org/10.1603/0022-0493(2007)100[1577:EPEABC]2.0.CO;2.CrossRefGoogle ScholarPubMed
Michigan State University Enviroweather. 2024. Weather-based pest, natural resources, and production tools. Michigan State University, East Lansing, Michigan, United States of America. Available from https://www.enviroweather.msu.edu/ [accessed 1 January 2020].Google Scholar
Petrice, T.R., Poland, T.M., Bauer, L.S., Strazanac, J.S., Duan, J.J., Schmude, J.M., and Ravlin, F.W. 2023. Factors affecting yellow pan trap captures of the emerald ash borer biocontrol agents Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae) and Spathius galinae Belokobylskij & Strazanac (Hymenoptera: Braconidae): implications for monitoring establishment. Biological Control, 184: 105272. https://doi.org/10.1016/j.biocontrol.2023.105272.CrossRefGoogle Scholar
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. thesis. University of Toronto, Toronto, Canada.Google Scholar
Roscoe, L.E., Lyons, D.B., and Smith, S.M. 2016. Observations on the life-history traits of the North American parasitoid Phasgonophora sulcata Westwood (Hymenoptera: Chalcididae) attacking Agrilus planipennis (Coleoptera: Buprestidae) in Ontario, Canada. The Canadian Entomologist, 148: 294–306. https://doi.org/10.4039/tce.2015.72.CrossRefGoogle Scholar
SAS Institute. 2012. OCUser’s Manual. Version 9.4. SAS Institute, Cary, North Carolina, United States of America. Available from https://documentation.sas.com/doc/en/pgmsascdc/9.4_3.5/shrref/titlepage.htm [accessed 30 October 2024].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, 2012: 813929. https://doi.org/10.1155/2012/813929.Google Scholar
United States Department of Agriculture, Animal and Plant Health Inspection Service–Agricultural Research Service–Forest Service. 2021. Emerald ash borer biological control release and recovery guidelines. United States Department of Agriculture, Riverdale, Maryland, United States of America. Available from https://www.aphis.usda.gov/sites/default/files/eab-field-release-guidelines.pdf. [accessed 30 October 2024].Google Scholar
Yang, Z.-Q., Strazanac, J.S., Marsh, P.M., Van Achterberg, C., and Choi, W.-Y. 2006. 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. https://doi.org/10.1603/0013-8746(2005)098[0636:frpfco]2.0.co;2.CrossRefGoogle Scholar