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Lysiphlebus orientalis (Hymenoptera, Braconidae), a new invasive aphid parasitoid in Europe – evidence from molecular markers

Published online by Cambridge University Press:  01 March 2013

Andjeljko Petrović*
Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia
Milana Mitrović
Department of Plant Pests, Institute for Plant Protection and Environment, Banatska 33, Zemun, Serbia
Petr Starý
Laboratory of Aphidology, Institute of Entomology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, 37005 České Budějovice, Czech Republic
Olivera Petrović-Obradović
Department of Plant Protection, Faculty of Agriculture, University of Belgrade, Nemanjina 6, 11081 Zemun, Serbia
Vladimir Žikić
Department of Biology and Ecology, Faculty of Sciences and Mathematics, University of Niš, Višegradska 33, 18000 Niš, Serbia
Željko Tomanović
Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade, Serbia
Christoph Vorburger
Institute of Integrative Biology, ETH Zürich, Switzerland, and EAWAG, Swiss Federal Institute of Aquatic Science and Technology, Überlandstrasse 133, 8600 Dübendorf, Switzerland
*Author for correspondence Phone: +381 11 2638 890 Fax: +381 11 2638 500 E-mail:


We report the occurrence of Lysiphlebus orientalis in Serbia, an aphid parasitoid from the Far East that is new to Europe and has the potential to become invasive. Our finding based on morphological characters is confirmed by analyses of mitochondrial cytochrome oxidase subunit I sequences. An increase in number and an expansion of the host range were observed during field studies over the past two years, and it is determined that the current host range encompasses nine aphid hosts on 12 different host plants, forming 13 tri-trophic associations. A host range determined for European populations of L. orientalis appears wider compared with that in its Far Eastern native habitats where Aphis glycines Mats. is the sole known host. Moreover, it overlaps considerably with the host ranges of European parasitoids that play an important role in the natural control of pest aphids.

Research Paper
Copyright © Cambridge University Press 2013 

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Boivin, G., Hance, T. & Brodeur, J. (2012) Aphid parasitoids in biological control. Canadian Journal of Plant Science 92, 112.Google Scholar
Brewer, M.J. & Elliott, N.C. (2004) Biological control of cereal aphids in North America and mediating effects of host plant and habitat manipulations. Annual Review of Entomology 49, 219242.Google Scholar
Cecilio, A. (1994) Faunistic evolution after the introduction of Lysiphlebus testaceipes (Cresson) (Hymenoptera: Aphidiidae) in Portugal, and its importance for the control of aphids. Boletín de Sanidad Vegetal Plagas 20, 471476.Google Scholar
Derocles, S.A., LE Ralec, A., Plantegenest, M., Chaubet, B., Cruaud, C., Cruaud, A. & Rasplus, J.Y. (2011) Identification of molecular markers for DNA barcoding in the Aphidiinae (Hym. Braconidae). Molecular Ecology Resources 12, 197208.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294297.Google Scholar
Hagvar, E.B. & Hofsvang, T. (1991) Aphid parasitoids (Hymenoptera: Aphidiidae): biology, host selection and use in biological control. Biocontrol News and Information 12, 1341.Google Scholar
Hallman, G.J. & Schwalbe, C.P. (2002) Invasive Arthropods in Agriculture: Problems and Solutions. Enfield, NH, USA, Science Publishers Inc.Google Scholar
Heimpel, G.E., Frelich, L.E., Landis, D.A., Hopper, K.R., Hoelmer, K.A., Sezen, Z., Asplen, M.K. & Wu, K. (2010) European buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America. Biological Invasions 12, 29132931.Google Scholar
Kaiser, M.C. & Heimpel, G.E. (2011) Unexpected risk: how parasitoid induced maternal effects may upset biological control. In Proceedings of the Meeting of Entomological Society of America, North Central Branch, March 13–16, 2011, Minneapolis, MN, Entomological Society of America. Available online at (accessed 30 June 2012).Google Scholar
Kambhampati, S., Voelkl, W. & Mackauer, M. (2000) Phylogenetic relationships among genera of Aphidiinae (Hymenoptera: Braconidae) based on DNA sequence of the mitochondrial 16S rRNA gene. Systematic Entomology 25, 437445.Google Scholar
Kavallieratos, N.G., Tomanović, Ž., Starý, P., Athanassiou, C.G., Sarlis, G.P., Petrović, O., Niketić, M. & Veroniki, M.A. (2004) A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of southeastern Europe and their aphid-plant associations. Applied Entomology and Zoology 39, 527563.Google Scholar
Mackauer, M. (1961) Die Typen der Unterfamilie Aphidiinae des Britischen Museums London (Hymenoptera: Braconidae). Beitraege zur Entomologie 11, 96154.Google Scholar
Maynard Smith, M.J. (1978) The Evolution of Sex. Cambridge, Cambridge University Press.Google Scholar
Nyabuga, F.N., Loxdale, H.D., Sharbel, T.F., Todd, M. & Weisser, W.W. (2009) Microsatellites from Lysiphlebus hirticornis Mackauer (Hymenoptera: Braconidae), a specialist primary parasitoid attacking the specialist tansy aphid, Metopeurum fuscoviride Stroyan (Hemiptera: Aphididae). Molecular Ecology Resources 9, 931934.Google Scholar
Petrović, A., Tomanović, Ž., Žikić, V., Kavallieratos, N.G. & Starý, P. (2009) New records of Aphidiinae (Hymenoptera: Braconidae) from Serbia and Montenegro. Acta Entomolgica Serbica 14, 219224.Google Scholar
Petrović, A., Žikić, V., Petrović-Obradović, O., Mitrovski Bogdanović, A., Kavallieratos, N.G., Starý, P. & Tomanović, Ž. (2011) Two new species of aphid parasitoids (Hymenoptera, Braconidae, Aphidiinae) from the Balkan Peninsula. Zootaxa 2895, 5864.Google Scholar
Pike, K., Starý, P., Miller, T., Graf, G., Allison, D., Boydston, L. & Miller, R. (2000) Aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Northwest USA. Proceedings of the Entomological Society of Washington 102, 699740.Google Scholar
Ragsdale, D.W., Landis, D.A., Brodeur, J., Heimpel, G.E. & Desneux, N. (2011) Ecology and management of the soybean aphid in North America. Annual Review of Entomology 56, 375399.Google Scholar
Roy, H.E., Roy, D.B. & Roques, A. (2011) Inventory of terrestrial alien arthropod predators and parasites established in Europe. BioControl 56, 477504.CrossRefGoogle Scholar
Sandrock, C., Schirrmeister, B. & Vorburger, C. (2011) Evolution of reproductive mode variation and host associations in a sexual-asexual complex of aphid parasitoids. BMC Evolutionary Biology 11, 348. doi:10.1186/1471-2148-11-348.Google Scholar
Shea, K. & Chesson, P. (2002) Community ecology theory as a framework for biological invasions. Trends in Ecology & Evolution 17, 170176.Google Scholar
Starý, P. (2006) Aphid parasitoids of the Czech Republic (Hymenoptera: Braconidae: Aphidiinae). Praha, Czech Republic, Academia.Google Scholar
Starý, P. & Lukáš, J. (2009) Aphid parasitoids and their tritrophic associations in Slovakia (Hymenoptera: Braconidae, Aphidiinae). Acta Hymenopterologica Slovaca 1, 163.Google Scholar
Starý, P., Lyon, J.P. & Leclant, F. (1988) Post-colonisation host range of Lysiphlebus testaceipes (Cresson) in the mediterranean area (Hymenoptera, Aphidiidae). Acta Entomologica Bohemoslovaca 85, 111.Google Scholar
Starý, P., Lumbierres, B. & Pons, X. (2004) Opportunistic changes in the host range of Lysiphlebus testaceipes (Cr.), an exotic aphid parasitoid expanding in the Iberian Peninsula. Journal of Pest Science 77, 139144.Google Scholar
Starý, P., Rakhshani, E., Tomanović, Ž., Hoelmer, K., Kavallieratos, N.G., Yu, J., Wang, M. & Heimpel, G.E. (2010) A new species of Lysiphlebus Förster 1862 (Hymenoptera: Braconidae: Aphidiinae) attacking soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae) from China. Journal of Hymenoptera research 19, 179186.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739.Google Scholar
van Achterberg, C. (2011) Fauna Europaea: Hymenoptera: Braconidae. Fauna Europaea version 2.4. Available online at (accessed 29 June 2012).Google Scholar