Skip to main content
SpringerLink
Log in

Intraguild predation between the invasive ladybird Harmonia axyridis and non-target European coccinellid species

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The coccinellid Harmonia axyridis (Pallas) has been used for augmentative and classical biological control in many environments. More recently it has invaded large parts of Europe and negative effects for native populations of aphidophagous coccinellids are beginning to emerge. Here we investigate intraguild predation (IGP) between H. axyridis and eleven native non-target European coccinellids, including less common species which have not been studied so far within this context of non-target effects. When first-instars of H. axyridis were paired with the native species, only Anatis ocellata (Linnaeus) and Calvia quatuordecimguttata (L.) were significantly superior to the former whereas H. axyridis was superior in three cases, i.e. against Aphidecta obliterata (L.), Coccinella septempunctata L. and Hippodamia variegata (Goeze). Non-significant results were obtained for all other pairings. Similar tests with the fourth larval instar revealed stronger IGP rates and H. axyridis was found to be superior in the interactions with Adalia bipunctata (L.), Adalia decempunctata (L.), A. obliterata, Calvia decemguttata (L.), C. quatuordecimguttata, C. septempunctata, H. variegata, Oenopia conglobata (L.) and Propylea quatuordecimpunctata (L.) whereas non-significant results were obtained for interactions with two other native species. Another experiment revealed that H. axyridis was able to prey more successfully upon egg of most native coccinellid species than vice versa. However, C. quatuordecimguttata eggs seem to be more protected against predation than those of the other species. Survival of first-instar H. axyridis was higher on conspecific eggs compared to eggs of any other species tested. Our results suggest that H. axyridis may become a threat to a wide range of native aphidophagous coccinellids sharing similar ecological niches except species showing high potential for chemical or physical protection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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 53:69–88

    Article  Google Scholar 

  • Agarwala BK, Dixon AFG (1991) Cannibalism and interspecific predation in ladybirds. In: Pogar L, Chambers R, Dixon AFG, Hodek I (eds) Behaviour and impact of aphidophaga. SPB Academic Publishers, The Hague, The Netherlands, pp 95–102

  • Alyokhin A, Sewell G (2004) Changes in a lady beetle community following the establishment of three alien species. Biol Invasions 6:463–471

    Article  Google Scholar 

  • Babendreier D (2007) Pros and cons of biological control. In: Nentwig W (ed) Biological invasions. Springer, Berlin, Germany, pp 403–418

  • Blum MS, Hilker M (2002) Chemical protection of insect eggs. In: Hilker M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell, Berlin, Germany, pp 61–90

  • Brown PMJ, Adriaens T, Bathon H, Cuppen J, Goldarazena A, Hägg T, Kenis M, Klausnitzer BE, Kovar I, Loomans AJ, Majerus MEN, Nedved O, Pedersen J, Rabitsch W, Roy HE, Ternois V, Zakharov I, Roy DB (2008) Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl 53:5–21

    Article  Google Scholar 

  • Chapin JB, Brou VA (1991) Harmonia axyridis (Pallas), the third species of the genus to be found in the United States (Coleoptera: Coccinellidae). Proc Entomol Soc Wash 93:630–635

    Google Scholar 

  • 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 27:1574–1580

    Google Scholar 

  • Cottrell TE (2004) Suitability of exotic and native lady beetle eggs (Coleoptera: Coccinellidae) for development of lady beetle larvae. Biol Control 31:362–371

    Article  Google Scholar 

  • De Clercq P, Mason PG, Babendreier D (2011) Benefits and risks of exotic biological control agents. BioControl 56:681–698

    Article  Google Scholar 

  • Dixon AFG (2000) Insect predator-prey dynamics: ladybird beetles and biological control. Cambridge University Press, Cambridge, UK

  • Doumbia M, Hemptinne JL, Dixon AFG (1998) Assessment of patch quality by ladybirds: role of larval tracks. Oecologia 113:197–202

    Article  Google Scholar 

  • Evans EW (2004) Habitat displacement of North American ladybirds by an introduced species. Ecology 85:637–647

    Article  Google Scholar 

  • Fauna Europaea (2012) Fauna Europaea version 2.4. http://www.faunaeur.org. Accessed 28 May 2012

  • Félix S, Soares AO (2004) Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): the role of body weight. Eur J Entomol 101:237–242

    Google Scholar 

  • Gordon RD (1985) The Coleoptera (Coccinellidae) of America north of Mexico. J N Y Entomol Soc 93:1–912

    Google Scholar 

  • Harmon JP, Stephens E, Losey J (2007) The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. J Insect Conserv 11:85–94

    Article  Google Scholar 

  • Hautier L, Grégoire JC, de Schauwers J, San Martin G, Callier P, Jansen JP, de Biseau JC (2008) Intraguild predation by Harmonia axyridis on coccinellids revealed by exogenous alkaloid sequestration. Chemoecology 18:191–196

    Article  CAS  Google Scholar 

  • Hautier L, San Martin y Gomez G, Callier P, de Biseau J, Gregoire J (2011) Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field. Biol Invasions 13:1805–1814

    Article  Google Scholar 

  • Hemptinne JL, Dixon AFG (2000) Defence, oviposition and sex: semiochemical parsimony in two species of ladybird beetles (Coleoptera, Coccinellidae)? A short review. Eur J Entomol 97:443–447

    CAS  Google Scholar 

  • Hemptinne JL, Lognay G, Gauthier C, Dixon AFG (2000) Role of surface chemical signals in egg cannibalism and intraguild predation in ladybirds (Coleoptera: Coccinellidae). Chemoecology 10:123–128

    Article  CAS  Google Scholar 

  • Howarth FG (1991) Environmental impacts of classical biological control. Annu Rev Entomol 36:485–509

    Article  Google Scholar 

  • Janssen A, Montserrat M, HilleRisLambers R, de Roos AM, Pallini A, Sabelis MW (2006) Intraguild predation usually does not disrupt biological control. In: Brodeur J, Boivin G (eds) Trophic and guild interactions in biological control, vol 3. Springer, Dordrecht, The Netherlands, pp 21–44

  • Janssen A, Sabelis MW, Magalhães S, Montserrat M, van der Hammen T (2007) Habitat structure affects intraguild predation. Ecology 88:2713–2719

    Article  PubMed  Google Scholar 

  • Kalaskar A, Evans EW (2001) Larval responses of aphidophagous ladybeetles (Coleoptera: Coccinellidae) to weevil larvae versus aphids as prey. Ann Entomol Soc Am 94:76–81

    Article  Google Scholar 

  • Katsoyannos P, Kontodimas DC, Stathas GJ, Tsartsalis CT (1997) Establishment of Harmonia axyridis on citrus and some data on its phenology in Greece. Phytoparasitica 25:183–191

    Article  Google Scholar 

  • Kenis M, Adriaens T, Brown P, Katsanis A, van Vlaenderen J, Eschen R, Golaz L, Zindel R, San Martin y Gomez G, Babendreier D, Ware R (2010) Impact of Harmonia axyridis on European ladybirds: Which species are most at risk? IOBC/WPRS Bull 58:57–59

    Google Scholar 

  • Klausnitzer B, Klausnitzer H (1997) Marienkäfer. Neue Brehm-Bücherei, Magdeburg, Germany

  • Koch RL (2003) The multicoloured Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control and non-target impacts. J Insect Sci 3:1–16

    Article  Google Scholar 

  • Lucas E (2005) Intraguild predation among aphidophagous predators. Eur J Entomol 102:351–364

    Google Scholar 

  • Lucas E, Coderre D, Vincent C (1997) Voracity and feeding preferences of two aphidophagous coccinellids on Aphis citricola and Tetranychus urticae. Entomol Exp Appl 85:151–159

    Article  Google Scholar 

  • Majerus MEN (1994) Ladybirds (No. 81, new naturalist series). HarperCollins, London, UK

  • McClure MS (1986) Role of predators in regulation of endemic populations of Matsucoccus matsumarae (Homoptera: Margarodidae) in Japan. Environ Entomol 15:976–983

    Google Scholar 

  • McClure MS (1987) Potential of the Asian predator, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), to control Matsucoccus resinosae Bean and Godwin (Homoptera: Margarodidae) in the United States. Environ Entomol 16:224–230

    Google Scholar 

  • Meisner M, Harmon JP, Harvey CT, Ives AR (2011) Intraguild predation on the parasitoid Aphidius ervi by the generalist predator Harmonia axyridis: the threat and its avoidance. Entomol Exp Appl 138:193–201

    Article  Google Scholar 

  • Michaud JP (2002) Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Environ Entomol 31:827–835

    Article  Google Scholar 

  • Michaud JP (2003) A comparative study of larval cannibalism in three species of ladybeetle (Coleoptera: Coccinellidae). Ecol Entomol 28:92–101

    Article  Google Scholar 

  • Michaud JP, Grant AK (2003) Intraguild predation among ladybeetles and a green lacewing: Do the larval spines of Curinus coeruleus (Coleoptera: Coccinellidae) serve a defensive function? Bull Entomol Res 93:499–505

    Article  PubMed  CAS  Google Scholar 

  • Michaud JP, Grant AK (2004) The adaptive significance of sibling egg cannibalism in the Coccinellidae: comparative evidence from three species. Ann Entomol Soc Am 97:710–719

    Article  Google Scholar 

  • Omkar Pervez A, Gupta K (2006) Why do neonates of aphidophagous ladybird beetles preferentially consume conspecific eggs in presence of aphids? Biocontrol Sci Technol 16:233–243

    Article  Google Scholar 

  • Osawa N (1992) Sibling cannibalism in the ladybird beetle Harmonia axyridis Pallas: fitness consequences for mother and offspring. Res Popul Ecol 34:45–55

    Article  Google Scholar 

  • Pasteels JM, Deroe C, Tursch B, Braekman JC, Daloze D, Hootele C (1973) Distribution et activités des alcaloïdes défensifs des Coccinellidae. J Insect Physiol 19:1771–1784

    Article  CAS  Google Scholar 

  • Pell JK, Baverstock J, Roy HE, Ware RL, Majerus MEN (2008) Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl 53:147–168

    Article  Google Scholar 

  • Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330

    Article  Google Scholar 

  • Rosenheim JA, Wilhoit LR, Armer CA (1993) Influence of intraguild predation among insect predators on the suppression of a herbivore population. Oecologia 96:439–449

    Article  Google Scholar 

  • Roy HE, Baverstock J, Ware RL, Clark SJ, Majerus MEN, Baverstock KE, Pell JK (2008) Intraguild predation of the aphid pathogenic fungus Pandora neoaphidis by the invasive coccinellid Harmonia axyridis. Ecol Entomol 33:1–8

    Article  Google Scholar 

  • Roy HE, Adriaens T, Isaac NJB, Kenis M, Onkelinx T, San Martin G, Brown PMJ, Hautier L, Poland R, Roy DB, Comont R, Eschen R, Frost R, Zindel R, van Vlaenderen J, Nedvěd O, Ravn HP, Grégoire J-C, de Biseau J-C, Maes D (2012) Invasive alien predator causes rapid declines of native European ladybirds. Divers Distrib 18:717–725

    Google Scholar 

  • Sato S, Dixon AFG (2004) Effect of intraguild predation on the survival and development of tree species of aphidophagous ladybirds: consequences for invasive species. Agric For Entomol 6:21–24

    Article  Google Scholar 

  • Sato S, Yasuda H, Evans EW (2005) Dropping behaviour of larvae of aphidophagous ladybirds and its effect 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 30:220–224

    Article  Google Scholar 

  • Savoiskaya GI, Klausnitzer B (1973) In: Hodek I (ed) Biology of Coccinellidae. Academia Publishing House of the Czechoslovak Academy of Sciences, Prague, Czech Republic, pp 36–55

  • Sebolt DC, Landis DA (2004) Arthropod predators of Galerucella calmariensis L. (Coleoptera: Chrysomelidae): an assessment of biotic interference. Environ Entomol 33:356–361

    Article  Google Scholar 

  • Simberloff D (1992) Conservation of pristine habitats and unintended effects of biological control. In: Kaufmann WC, Nechols JE (eds) Selection criteria and ecological consequences of importing natural enemies. ESA, Lanham, USA, pp 103–117

  • Snyder WE (2009) Coccinellids in diverse communities: Which niche fits? Biol Control 51:323–335

    Article  Google Scholar 

  • Snyder WE, Joseph SB, Preziosi RF, Moore AJ (2000) Nutritional benefits of cannibalism for the lady beetle Harmonia axyridis (Coleoptera: Coccinellidae) when prey quality is poor. Environ Entomol 29:1173–1179

    Article  Google Scholar 

  • Ueno H, Sato Y, Tsuchida K (1998) Colour-associated mating success in a polymorphic ladybird beetle, Harmonia axyridis. Funct Ecol 12:757–761

    Article  Google Scholar 

  • van Driesche RG, Carruthers RI, Center T, Hoddle MS, Hough-Goldstein J, Morin L, Smith L, Wagner DL, Blossey B, Brancatini V, Casagrande R, Causton CE, Coetzee JA, Cuda J, Ding J, Fowler SV, Frank JH, Fuester R, Goolsby J, Grodowitz M, Heard TA, Hil MP, Hoffmann JH, Huber J, Julien M, Kairo MTK, Kenis M, Mason P, Medal J, Messing R, Miller R, Moore A, Neuenschwander P, Newman R, Norambuena H, Palmer WA, Pemberton R, Perez Panduro A, Pratt PD, Rayamajhi M, Salom S, Sands D, Schooler S, Sheppard A, Shaw R, Schwarzländer M, Tipping PW, van Klinken RD (2010) Classical biological control for the protection of natural ecosystems: past achievements and current efforts. Biol Control 54:S2–S33

    Article  Google Scholar 

  • van Lenteren JC (ed) (2008) IOBC Internet book of biological control. http://www.iobc-global.org/download/IOBC%20InternetBookBiCoVersion5January2008.pdf. Accessed 28 May 2012

  • Vance-Chalcraft HD, Rosenheim JA, Vonesh JR, Osenberg WC, Sih A (2007) The influence of intraguild predation on aphid suppression and prey release: a meta-analysis. Ecology 88:2689–2696

    Article  PubMed  Google Scholar 

  • Ware RL, Majerus MEN (2008) Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. BioControl 53:169–188

    Google Scholar 

  • Ware RL, Evans N, Malpas L, Michie LJ, O’Farrell K, Majerus MEN (2008a) Intraguild predation of British and Japanese coccinellid eggs by the invasive ladybird Harmonia axyridis. Neobiota 7:263–275

    Google Scholar 

  • Ware RL, Ramon-Portugal F, Magro A, Ducamp C, Hemptinne JL, Majerus MEN (2008b) Chemical protection of Calvia quatuordecimguttata eggs against intraguild predation by the invasive ladybird Harmonia axyridis. BioControl 53:189–200

    Article  Google Scholar 

Download references

Acknowledgments

The authors wish to acknowledge the help of Mr. Johan van Vlaenderen for assistance in collecting coccinellids and in laboratory work. We are grateful to Dr. Christelle Péré, Ms. Natalia Guazzone, Mr. Ioan-Sorin Sirbu and Ms. Luma Delaplace for assistance in maintaining the cultures of aphids and coccinellids. We are also thankful to the late Dr. Mike Majerus and Dr. Remy Poland for helpful discussions and to Mr. Louis Hautier for providing us cultures of aphids. We thank the anonymous reviewers for their very helpful comments on the manuscript. This study was funded by the Swiss National Science Foundation (Grant 3100A0-117831/1).

Author information

Authors and Affiliations

  1. CABI Europe-Switzerland, Rue des Grillons 1, 2800, Delémont, Switzerland

    Angelos Katsanis, Dirk Babendreier & Marc Kenis

  2. Community Ecology, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, 3012, Bern, Switzerland

    Wolfgang Nentwig

  3. Department of Ecology and Evolution, University of Lausanne, UNIL Sorge, Le Biophore, 1015, Lausanne, Switzerland

    Angelos Katsanis

Authors
  1. Angelos Katsanis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dirk Babendreier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wolfgang Nentwig
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marc Kenis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Angelos Katsanis.

Additional information

Handling Editor: Arne Janssen

Rights and permissions

Reprints and permissions

About this article

Cite this article

Katsanis, A., Babendreier, D., Nentwig, W. et al. Intraguild predation between the invasive ladybird Harmonia axyridis and non-target European coccinellid species. BioControl 58, 73–83 (2013). https://doi.org/10.1007/s10526-012-9470-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-012-9470-2

Keywords

Search

Navigation