Biological Invasions

, Volume 13, Issue 8, pp 1805–1814 | Cite as

Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field

  • Louis Hautier
  • Gilles San Martin
  • Pierre Callier
  • Jean-Christophe de Biseau
  • Jean-Claude Grégoire
Original Paper


Over a period of less than 5 years, Belgium was thoroughly invaded by the multicolored Asian coccinellid, Harmonia axyridis. At the same time, a decline of some native coccinellid species was observed in tree habitats. One hypothesis about the cause of this decline was that it might have been due to intraguild predation (IGP) by H. axyridis. In natural conditions, IGP between coccinellids can be tracked by using defensive compounds. Exogenous alkaloids in H. axyridis were therefore examined by gas chromatography-mass spectrometry (GC–MS), using individuals sampled from lime trees that were also occupied by other species of coccinellids. Harmonia axyridis was the dominant species at all life stages, in terms of both numbers of sites occupied and local abundance. The GC–MS analysis of H. axyridis larvae revealed traces of exogenous alkaloids from 19 of the 20 sites and, in nine of those 19 sites, more than 30% of the larvae analyzed contained exogenous alkaloids. Three alkaloids were detected: adaline from Adalia spp., calvine from Calvia spp. and propyleine from Propylea quatuordecimpunctata. Predation by H. axyridis on two different coccinellid species was also detected in the same larva, reinforcing the status of H. axyridis as a top predator. A generalized linear model indicated that IGP frequency was positively influenced by two variables: the abundance of extraguild and intraguild prey; and the interaction between these two variables. Our results therefore support the hypothesis that IGP by H. axyridis on native coccinellids in tree habitats has led to the decline of several of these species.


Alkaloids Biological control Biological invasions Ladybirds Gut content Native species decline 



We thank Laurent Grumiau for his valuable technical assistance in the GC–MS analyses. We would also like to thank Helen Roy for proofreading the manuscript and two anonymous reviewers for helpful comments. This research was supported by the Fonds National de la Recherche Scientifique (grant FRFC 2.4615.06), and by the Agence Nationale de la Recherche, France (ANR, project BioInv-4I).


  1. Adriaens T, Branquart E, Maes D (2003) The multicoloured Asian ladybird Harmonia axyridis Pallas (Coleoptera: Coccinellidae), a threat for native aphid predators in Belgium? Bel J Zool 133:195–196Google Scholar
  2. Adriaens T, San Martin y Gomez G, Maes D (2008) Invasion history, habitat preferences and phenology of the invasive ladybird Harmonia axyridis in Belgium. Biocontrol 53:69–88CrossRefGoogle Scholar
  3. Adriaens T, San Martin G, Hautier L, Branquart E, Maes D (2010) Toward a Noah’s Ark for native ladybirds in Belgium? Working Group Benefits and Risks of Exotic Biological Control Agents. IOBC/wprs Bulletin 58 1–3Google Scholar
  4. Alyokhin A, Sewell G (2004) Changes in a lady beetle community following the establishment of three alien species. Biol Invasions 6:463–471CrossRefGoogle Scholar
  5. Baugnée JY, Branquart E (2000) Clef de terrain pour la reconnaissance des principales coccinelles de Wallonie (Chilocorinae, Coccinellinae & Epilachninae). Jeunes & Nature asbl. Document réalisé en collaboration avec la FUSAGx (Unité de Zoologie générale et appliquée) et publié à l’aide de la Région wallonne (DGRNE)Google Scholar
  6. Brown P, Adriaens T, Bathon H, Cuppen J, Goldarazena A, Hägg T, Kenis M, Klausnitzer B, Kovář I, Loomans A, Majerus M, Nedved O, Pedersen J, Rabitsch W, Roy H, Ternois V, Zakharov I, Roy D (2008) Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. Biocontrol 53:5–21CrossRefGoogle Scholar
  7. Burgio G, Santi F, Maini S (2002) On intra-guild predation and cannibalism in Harmonia axyridis (Pallas) and Adalia bipunctata L. (Coleoptera: Coccinellidae). Biol Control 24:110–116CrossRefGoogle Scholar
  8. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York, USAGoogle Scholar
  9. Colunga-Garcia M, Gage SH (1998) Arrival, establishment, and habitat use of the multicolored Asian lady beetle (Coleoptera: Coccinellidae) in a Michigan landscape. Environ Entomol 27:1574–1580Google Scholar
  10. Cottrell TE, Yeargan KV (1998) Intraguild predation between an Introduced Lady Beetle, Harmonia axyridis (Coleoptera: Coccinellidae), and a Native Lady Beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). J Kansas Entomol Soc 71:159–163Google Scholar
  11. Daloze D, Braekman J, Pasteels JM (1994) Ladybird defence alkaloids: structural: chemotaxonomic and biosynthetic aspects (Col.: Coccinellidae). Chemoecology 5:173–183CrossRefGoogle Scholar
  12. Dixon AFG (1971) The role of intra-specific mechanisms and predation in regulating the numbers of the lime aphid, Eucallipterus tiliae L. Oecologia 8:179–193CrossRefGoogle Scholar
  13. Dixon AF (1998) Aphid ecology: an optimization approach. Chapman and Hall, London, UKGoogle Scholar
  14. Dixon AF (2000) Insect predator-prey dynamics: ladybird beetles and biological control. Cambridge University Press, Cambridge, UKGoogle Scholar
  15. Dobson AJ (2002) An introduction to generalized linear models. CRC Press, Boca Raton, FL, USAGoogle Scholar
  16. Elliott N, Kieckhefer R, Kauffman W (1996) Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia 105:537–544CrossRefGoogle Scholar
  17. Evans EW (2004) Habitat displacement of North American ladybirds by an introduced species. Ecology 85:637–647CrossRefGoogle Scholar
  18. Gardiner M, Landis D (2007) Impact of intraguild predation by adult Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Hemiptera: Aphididae) biological control in cage studies. Biol Control 40:386–395CrossRefGoogle Scholar
  19. Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, Cambridge, UKGoogle Scholar
  20. Glisan King A, Meinwald J (1996) Review of the defensive chemistry of Coccinellids. Chem Rev 96:1105–1122PubMedCrossRefGoogle Scholar
  21. Hautier L, Grégoire J, de Schauwers J, San Martin G, Callier P, Jansen J, de Biseau J (2008) Intraguild predation by Harmonia axyridis on coccinellids revealed by exogenous alkaloid sequestration. Chemoecology 18:191–196CrossRefGoogle Scholar
  22. Hindayana D, Meyhöfer R, Scholz D, Poehling HM (2001) Intraguild predation among the hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and other aphidophagous predators. Biol Control 20:236–246CrossRefGoogle Scholar
  23. Hironori Y, Katsuhiro S (1997) Cannibalism and interspecific predation in two predatory ladybirds in relation to prey abundance in the field. Biocontrol 42:153–163Google Scholar
  24. Honěk A (1985) Habitat preferences of aphidophagous coccinellids [Coleoptera]. Biocontrol 30:253–264Google Scholar
  25. Iablokoff-Khnzorian SM (1982) Les coccinelles, Coléoptères-Coccinellidae: tribu coccinellini des régions paléarctique et orientale. Société nouv. des Editions Boubée, ParisGoogle Scholar
  26. Jansen J, Hautier L (2008) Ladybird population dynamics in potato: comparison of native species with an invasive species, Harmonia axyridis. Biocontrol 53:223–233CrossRefGoogle Scholar
  27. Janssen A, Sabelis MW, Magalhães S, Montserrat M, van der Hammen T (2007) Habitat structure affects intraguild predation. Ecology 88:2713–2719PubMedCrossRefGoogle Scholar
  28. Kajita Y, Takano F, Yasuda H, Agarwala BK (2000) Effects of indigenous ladybird species (Coleoptera: Coccinellidae) on the survival of an exotic species in relation to prey abundance. Appl Entomol Zool 35:473–479CrossRefGoogle Scholar
  29. Laurent P, Braekman JC, Daloze D (2005) Insect chemical defense. Top Curr Chem 240:167–230Google Scholar
  30. Lucas E (2005) Intraguild predation among aphidophagous predators. Eur J Entomol 102:351–363Google Scholar
  31. Lucas E, Brodeur J (1999) Oviposition site selection by the predatory midge Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Environ Entomol 28:622–627Google Scholar
  32. Lucas E, Coderre D, Brodeur J (1998) Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79:1084–1092CrossRefGoogle Scholar
  33. Majerus MEN (1994) Ladybirds. The new naturalist series. Harper Collins Publishers, LondonGoogle Scholar
  34. Mills NJ (1982) Voracity, cannibalism and coccinellid predation. Ann Appl Biol 101:144–148Google Scholar
  35. Osawa N (1993) Population field studies of the aphidophagous ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae): life tables and key factor analysis. Popul Ecol 35:335–348CrossRefGoogle Scholar
  36. 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 53:147–168CrossRefGoogle Scholar
  37. Phoofolo MW, Obrycki JJ (1998) Potential for intraguild predation and competition among predatory Coccinellidae and Chrysopidae. Entomol Exp Appl 89:47–55 CrossRefGoogle Scholar
  38. Polis GA (1981) The evolution and dynamics of intraspecific predation. Annu Rev Ecol Syst 12:225–251CrossRefGoogle Scholar
  39. Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330CrossRefGoogle Scholar
  40. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL
  41. Rosenheim JA, Kaya HK, Ehler LE, Marois JJ, Jaffee BA (1995) Intraguild predation among biological-control agents: theory and evidence. Biol Control 5:303–335CrossRefGoogle Scholar
  42. Sato S, Yasuda H, Evans EW (2005) Dropping behaviour of larvae of aphidophagous coccinellids and its effects on incidence of intraguild predation: interactions between the intraguild prey, Adalia bipunctata (L.) and Coccinella septempunctata (L.), and the intraguild predator, Harmonia axyridis Pallas. Ecol Entomol 30:220–224CrossRefGoogle Scholar
  43. Sato S, Jimbo R, Yasuda H, Dixon AF (2008) Cost of being an intraguild predator in predatory coccinellids. Appl Entomol Zool 43:143–147CrossRefGoogle Scholar
  44. Sato S, Kushibuchi K, Yasuda H (2009) Effect of reflex bleeding of a predatory ladybird beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), as a means of avoiding intraguild predation and its cost. Appl Entomol Zool 44:203–206 CrossRefGoogle Scholar
  45. Schellhorn NA, Andow DA (1999) Cannibalism and interspecific predation: role of oviposition behavior. Ecol Appl 9:418–428Google Scholar
  46. Sloggett JJ, Davis AJ (2010) Eating chemically defended prey: alkaloid metabolism in an invasive coccinellid predator of other coccinellids (Coleoptera: Coccinellidae). J Exp Biol 213:237–241PubMedCrossRefGoogle Scholar
  47. Sloggett JJ, Obrycki JJ, Haynes KF (2009) Identification and quantification of predation: novel use of gas chromatography-mass spectrometric analysis of prey alkaloid marker. Funct Ecol 23:416–426CrossRefGoogle Scholar
  48. Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Annu Rev Ecol Syst 37:95–122CrossRefGoogle Scholar
  49. Soares A, Serpa A (2007) Interference competition between coccinellid beetle adults (Coleoptera: Coccinellidae): effects on growth and reproductive capacity. Popul Ecol 49:37–43CrossRefGoogle Scholar
  50. Takahashi K (1989) Intra- and inter-specific predations of lady beetles in spring alfalfa fields. Jpn J Entomol 57:199–203Google Scholar
  51. Tursch B, Daloze D, Hootele C (1972) The alkaloid of Propylaea quatuordecimpunctata L. (Coleoptera, Coccinellidae). Chimia 26:74–75Google Scholar
  52. Ware R, Majerus M (2008) Intraguild predation of immature stages of British and Japanese coccinellids by the invasive coccinellid Harmonia axyridis. Biocontrol 53:169–188CrossRefGoogle Scholar
  53. Ware R, Ramon-Portugal F, Magro A, Ducamp C, Hemptinne J, Majerus M (2008) Chemical protection of Calvia quatuordecimguttata eggs against intraguild predation by the invasive coccinellid Harmonia axyridis. Biocontrol 53:189–200CrossRefGoogle Scholar
  54. Weber DC, Lundgren JG (2009) Assessing the trophic ecology of the Coccinellidae: their roles as predators and as prey. Biol Control 51:199–214CrossRefGoogle Scholar
  55. Wratten SD (1973) The effectiveness of the Coccinellid Beetle. Adalia bipunctata (L.), as a predator of the lime aphid, Eucallipterus tiliae L. J Anim Ecol 42:785–802CrossRefGoogle Scholar
  56. Yasuda H, Ohnuma N (1999) Effect of cannibalism and predation on the larval performance of two coccinellid beetles. Entomol Exp Appl 93:63–67CrossRefGoogle Scholar
  57. Yasuda H, Kikuchi T, Kindlmann P, Sato S (2001) Relationships between attack and escape rates, cannibalism, and intraguild predation in larvae of two predatory coccinellids. J Insect Behav 14:373–384CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Louis Hautier
    • 1
    • 4
  • Gilles San Martin
    • 2
    • 3
  • Pierre Callier
    • 2
  • Jean-Christophe de Biseau
    • 2
  • Jean-Claude Grégoire
    • 4
  1. 1.Centre wallon de Recherches agronomiques, Département Sciences du vivantUnité Protection des plantes et écotoxicologieGemblouxBelgium
  2. 2.Evolution Biologique et EcologieUniversité Libre de BruxellesBrusselsBelgium
  3. 3.Earth and Life Institute, Biodiversity Research Centre, Behavioural Ecology and Conservation group Croix du Sud 4Universite catholique de LouvainLouvain-la-NeuveBelgium
  4. 4.Lutte biologique et Ecologie spatialeUniversité Libre de BruxellesBrusselsBelgium

Personalised recommendations