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30 In conclusion, using alkaloids as predation tracers allows to follow IGP interactions between H. axyridis and native coccinellids under field field conditions. This new detection technique is very sensitive and permits to detect the smallest prey that can be attacked by H. axyridis. The risk of detecting a contact instead of a predation event is very limited. In addition, exogenous alkaloids are persistent in the predators and can still be detected several days after an IGP event. Results from potato fields confirm that H. axyridis is an intraguild predator of native coccinelids (A. bipunctata, C. septempunctata, P. quatuordecimpunctata) under natural conditions. Acknowledgements We thank Evelyne Haulotte (Laboratory of Organic Chemistry, ULB) for the supply of synthetic adaline. Financial support was provided by the Belgian National Fund for Scientific Research, FNRS (grant FRFC 2.4615.06) References Daloze D., Braekman J. & Pasteels J.M., 1994. Ladybird defence alkaloids: Structural, chemotaxonomic and biosynthetic aspects (Col.: Coccinellidae). Chemoecology 5:173- 183. doi: 10.1007/BF01240602. Gagnon A.E., Heimpel G.E. & Brodeur J., 2005. Detection of intraguild predation between coccinellids using molecular analyses of gut-contents. International symposium on biological control of aphids and coccids (Tsuruoka, Japan). Hagler J.R., 2006. Development of an immunological technique for identifying multiple predator-prey interactions in a complex arthropod assemblage. Ann App Biol 149: 153- 165 Hautier L., Grégoire J., de Schauwers J., Martin G., Callier P., Jansen J. & de Biseau J., 2008. Intraguild predation by Harmonia axyridis on coccinellids revealed by exogenous alkaloid sequestration. Chemoecology 18:191-196. doi: 10.1007/s00049-008-0405-4. Harwood J.D. & Obrycki J.J., 2005. Quantifying aphid predation rates of generalist predators in the field. Eur. J. Entomol. 102: 335-350 Hoogendoorn M. & Heimpel G.E., 2001. PCR-based gut content analysis of insect predators: using ribosomal ITS-1 fragments from prey to estimate predation frequency. Mol Ecol 10: 2059-2067 Koch R.L., 2003. The multicolored Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non-target impacts. Journal of Insect Science 3:32. Pell J., Baverstock J., Roy H., Ware R. & Majerus M., 2008. Intraguild predation involving Harmonia axyridis : a review of current knowledge and future perspectives. BioControl 53:147-168. doi: 10.1007/s10526-007-9125-x. Triltsch H., 1999. Food remains in the guts of Coccinella septempunctata (Coleoptera: Coccinellidae) adults and larvae. Eur. J. Entomol. 96: 355-364 Ware R., & Majerus M., 2008. Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl 53:169- 188. doi: 10.1007/s10526-007-9135-8.
Measuring the impact of Harmonia axyridis intraguild predation on native coccinellids in the field Louis HAUTIER 1 , Jean-Claude GRÉGOIRE², Pierre CALLIER³, Gilles SAN MARTIN 3,4 Jean-Pierre JANSEN 1 & Jean-Christophe DE BISEAU 3 1 Département Lutte biologique et Ressources phytogénétiques, Centre wallon de Recherches agronomiques, Rue de Liroux, 2, B-5030 Gembloux, Belgium 2 Lutte biologique et Ecologie spatiale, Université Libre de Bruxelles, CP 160/12, Av. F.D. Roosevelt 50 – 1050, Brussels, Belgium 3 Eco-Ethologie évolutive, Université Libre de Bruxelles, CP 160/12, Av. F.D. Roosevelt 50 - 1050 Brussels, Belgium 4 Present address: Écologie comportementale et conservation de la biodiversité , BDIV , Université catholique de Louvain, Croix du Sud 4 B-1348 Louvain-la-Neuve, Belgium Introduction The Multicoloured Asian Ladybird, Harmonia axyridis Pallas, was introduced in 1997 in Belgium for aphid biological control (Adriaens et al. 2003). In less than five years, this ladybird has invaded the whole of Belgium in urban, agricultural and semi-natural habitats and has an overlapping niche with that of several native species (Adriaens et al. 2008). In parallel, a decline of native ladybird species such as Adalia bipunctata (L.) and Adalia decempunctata (L.), was observed in tree habitats in Brussels (San Martin et al. in prep). The causes of this decline are not clearly identified and could be due to competition with or to intraguild predation by, H. axyridis. Intraguild predation (IGP) is defined as “killing and eating of species that use similar resources” (Polis et al. 1989); this interaction is very frequent in aphidophagous guilds because aphids are limited resources (Lucas 2005). Several laboratory studies have reported that H. axyridis acts as an intraguild predator of Cecidomyiidae, Coccinellidae and Chrysopidae (Koch 2003, Pell et al. 2008, Ware & Majerus 2008), except for interactions with the ladybird Anatis ocelata (L.) (Ware & Majerus 2008). However, laboratory conditions are extreme circumstances for interactions and are considered a worst case. Under field conditions, IGP can be influenced by many factors such as extraguild prey (e.g; aphids), possibility of intraguild prey escape, and importance of niche overlap. To follow IGP by H. axyridis on native coccinellids in field conditions, a new method for detecting IGP was developed based on the detection of exogenous alkaloids from native ladybirds in H. axyridis larvae, using gas chromatography - mass spectrometry (Hautier et al., 2008). With this detection method, IGP by H. axyridis in lime trees (Tilia spp.) was studied in twenty sites in Brussels between June and July 2008. 40 to 110 branchs of lime tree, depending on site size, were beaten with a stick above a sweep net (65 cm in diameter and 130 cm in depth). H. axyridis larvae were isolated in microtubes and were kept in a freezer at -20°C until alkaloid analysis. 31
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