Hostname: page-component-848d4c4894-cjp7w Total loading time: 0 Render date: 2024-06-16T05:06:36.187Z Has data issue: false hasContentIssue false

Pre-release detection of a biocontrol agent: combining independent and public DNA sequences to identify the first North American record of Aulacidea pilosellae (Hymenoptera: Cynipidae)

Published online by Cambridge University Press:  11 August 2014

Chandra E. Moffat*
Department of Biology, University of British Columbia, Okanagan Campus, 3333 University Way, Kelowna, British Columbia, Canada
M. Alex Smith
Department of Integrative Biology, University of Guelph, Guelph, Ontario, Canada
2Corresponding author (e-mail:


Here we report the first North American detection of the gall wasp Aulacidea pilosellae Kieffer (Hymenoptera: Cynipidae), native to Central Europe and a promising candidate biological control agent for invasive hawkweeds (Pilosella Vaillant, Asteraceae) in North America. This occurrence was discovered through the intersection of (i) publically available DNA barcode data and (ii) DNA sequencing of a biocontrol agent before its release. COI DNA sequences of A. pilosellae collected in Central Europe were compared with publically available DNA sequence records. Despite the presence of other Aulacidea Ashmead in the database, the most similar sequence to the European A. pilosellae was an as yet unidentified specimen collected in the Ottawa Valley of eastern Ontario, Canada. Subsequent sequencing of a second gene region (28S-D2) of the Ottawa Valley specimen yielded an identical DNA sequence to the European A. pilosellae, confirming the presence of this species in Ontario. This note highlights the potential synergy that can result from making DNA barcode data publically available before formal taxonomic identification, and a new benefit of incorporating DNA sequencing of standardised markers into biological control programmes.

Physiology, Biochemistry, Development and Genetics – NOTE
© Entomological Society of Canada 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Subject Editor: Chris Schmidt


Ács, Z., Challis, R.J., Bihari, P., Blaxter, M., Hayward, A., Melika, G., et al. 2010. Phylogeny and DNA barcoding of inquiline oak gallwasps (Hymenoptera: Cynipidae) of the western Palaearctic. Molecular Phylogenetics and Evolution, 55: 210225.CrossRefGoogle ScholarPubMed
Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research, 25: 33893402.CrossRefGoogle ScholarPubMed
Argaman, Q. 1988. Additions to the cynipoid fauna of Israel (Hymenoptera, Cynipoidea). Israel Journal of Entomology, 22: 109118.Google Scholar
Benson, D.A., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., and Wheeler, D.L. 2008. GenBank. Nucleic Acids Research, 36: D25D30.CrossRefGoogle ScholarPubMed
Buhr, H. 1964. Bestimmungstabellen der Gallen (Zoo- und Phytocecidien) an Pflanzen Mittel- und Nordeuropas. Veb Gustav Fischer Verlag, Jena, Germany.Google Scholar
Dalla Torre, K.W. and Kieffer, J.J. 1910. Cynipidae. In Das Tierreich. Edited by F.E. Schultze. Liefer, Berlin, Germany. Pp. 1891.Google Scholar
deWaard, J.R., Humble, L.M., and Schmidt, B.C.S. 2010. DNA barcoding identifies the first North American records of the Eurasian moth, Eupithecia pusillata (Lepidoptera: Geometridae). Journal of the Entomological Society of British Columbia, 107: 2531.Google Scholar
deWaard, J.R., Landry, J.F., Schmidt, B.C., Derhousoff, J., McLean, J.A., and Humble, L.M. 2009. In the dark in a large urban park: DNA barcodes illuminate cryptic and introduced moth species. Biodiversity and Conservation, 18: 38253839.CrossRefGoogle Scholar
Eady, R.D. and Quinlan, J. 1963. Hymenoptera: Cynipoidea. Key to families and subfamilies and Cynipinae (including galls). Royal Entomological Society of London, London, United Kingdom.Google Scholar
Fernandez-Triana, J. 2010. Eight new species and an annotated checklist of Microgastrinae (Hymenoptera: Braconidae) from Canada and Alaska. ZooKeys, 63: 153. doi:10.3897/zookeys.63.565.CrossRefGoogle Scholar
Folliot, R. 1964. Contribution à l’étude de la biologie des Cynipides gallicoles (Hymenopteres: Cynipoidea). Annales des Sciences Naturelles Zoologie, 12: 407564.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3: 294299.Google ScholarPubMed
Gaskin, J.F., Bon, M.-C., Cock, M.J.W., Cristofaro, M., Biase, A.D., De Clerck-Floate, R., et al. 2011. Applying molecular-based approaches to classical biological control of weeds. Biological Control, 58: 121.CrossRefGoogle Scholar
Grosskopf, G., Wilson, L.M., and Littlefield, J.L. 2008. Host-range investigations of potential biological control agents of alien invasive hawkweeds (Hieracium spp.) in the USA and Canada: an overview. In Proceedings of the XII international symposium on biological control of weeds. Edited by M.H. Julien, R. Sforza, M.-C. Bon, H.C. Evans, P.E. Hatcher, H.L. Hinz, and B.G. Rector. CAB International, Wallingford, United Kingdom. Pp. 552557.Google Scholar
Heraty, J.M., Hawks, D., Kostecki, J.S., and Carmichael, A. 2004. Phylogeny and behavior of the Gollumiellinae, a new subfamily of the ant parasitic Eucharitidae (Hymenoptera: Chalcidoidea). Systematic Entomology, 29: 544559.CrossRefGoogle Scholar
Houard, C. 1913. Les Zoocécidies des plantes d’europe et du Bassin de la Méditerranée. Libraire Scientifique A. Hermann et Fils, Paris, France.Google Scholar
Humble, L.M., deWaard, J.R., and Quinn, M. 2009. Delayed recognition of the European poplar shoot borer, Gypsonoma aceriana (Duponchel) (Lepidoptera: Tortricidae) in Canada. Journal of the Entomological Society of British Columbia, 106: 6170.Google Scholar
Ionescu, M.A. 1957. Cynipinae. Fauna Republicii Populare Romine, Volume IX, Editura Academiei Republicii Populare Romine, Bucharest, Romania.Google Scholar
Ivanova, N.V., deWaard, J.R., and Hebert, P.D.N. 2006. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes, 6: 9981002.CrossRefGoogle Scholar
Moffat, C.E. 2012. Cryptic host-associated and frequency-dependent patterns of host species selection of a candidate weed biological control agent in its native range. Masters thesis. University of British Columbia. Available from [accessed 4 June 2014].Google Scholar
Moffat, C.E., Lalonde, R.G., Ensing, D.J., De Clerck-Floate, R.A., Grosskopf-Lachat, G., and Pither, J. 2013. Frequency-dependent host species use by a candidate biological control insect within its native European range. Biological Control, 67: 498508.CrossRefGoogle Scholar
Nieves-Aldrey, J.-L., Vardal, H., and Ronquist, F. 2005. Comparative morphology of terminal-instar larvae of Cynipoidea: phylogenetic implications. Zoologica Scripta, 34: 1536.CrossRefGoogle Scholar
Ratnasingham, S. and Hebert, P.D.N. 2007. BOLD: The Barcode of Life Data System ( Molecular Ecology Notes, 7: 355–364.Google Scholar
Ratnasingham, S. and Hebert, P.D.N. 2013. A DNA-based registry for all animal species: the barcode index number (BIN) system. Public Library of Science One, 8: e66213.Google ScholarPubMed
Sárospataki, M. 1999. Phytophagous insects associated with Hieracium pilosella (Asteraceae) in Hungary, Central Europe. Environmental Entomology, 28: 18.CrossRefGoogle Scholar
Saux, C., Fisher, B.L., and Spicer, G.S. 2004. Dracula ant phylogeny as inferred by nuclear 28S rDNA sequences and implications for ant systematics (Hymenoptera: Formicidae: Amblyoponinae). Molecular Phylogenetics and Evolution, 33: 457468.CrossRefGoogle ScholarPubMed
Sliva, M.D. and Shorthouse, J.D. 2006. Comparison of the development of stem galls induced by Aulacidea hieracii (Hymenoptera: Cynipidae) on hawkweed and by Diplolepis spinosa (Hymenoptera: Cynipidae) on rose. Canadian Journal of Botany, 84: 10521074.CrossRefGoogle Scholar
Smith, M.A., Rodriguez, J.J., Whitfield, J.B., Deans, A.R., Janzen, D.H., Hallwachs, W., et al. 2008. Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proceedings of the National Academy of Sciences, 105: 1235912364.CrossRefGoogle ScholarPubMed
Townes, H. 1962. Design for a Malaise trap. Proceeding of the Entomological Society Washington, 64: 253262.Google Scholar
Wellcome Trust 2011. Sharing data from large-scale biological research projects: a system of tripartite responsibility [online]. Report of a meeting organized by the Wellcome Trust, 14–15 January 2003, Fort Lauderdale, Florida, United States of America. Available from [accessed 1 May 2013.Google Scholar