Skip to main content
SpringerLink
Log in

A Well Protected Intruder: The Effective Antimicrobial Defense of the Invasive Ladybird Harmonia axyridis

  • Original Research
  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

The harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae) is a polyphagous predatory beetle native to Central and Eastern Asia. Since 2007 it has established all over Central Europe. In order to elucidate which defense strategy is responsible for its high resistance to diseases, we tested hemolymph as well as eleven main components of the headspace of H. axyridis for antimicrobial activity against Gram-positive (Bacillus subtilis, B. thuringiensis ssp. tenebrionis, Micrococcus luteus) and Gram-negative bacteria (Escherichia coli) and yeast (Saccharomyces cerevisiae). While three of the volatile compounds weakly reduced the growth of microorganisms, hemolymph of adults and larvae of H. axyridis strongly inhibited the growth of Gram-positive and Gram-negative bacteria as well as yeast. Furthermore, we compared the antimicrobial activity in the hemolymph of H. axyridis and Coccinella septempunctata. Antimicrobial activity in H. axyridis was about a thousand times higher compared to hemolymph from C. septempunctata. In contrast to C. septempunctata, the antimicrobial activity in H. axyridis was present without prior challenge. Minimal inhibitory concentration (MIC) of the hemolymph of H. axyridis was lowest against E. coli and yeast followed by B. subtilis, and was highest against entomopathogenic B. thuringiensis ssp. tenebrionidae. Furthermore, MIC values of the hemolymph obtained from live beetles were significantly lower than from frozen insects. This suggests that the active antimicrobial compound is affected by freezing and subsequent thawing of the beetles. Potential implications of our findings for the competitive advantages of H. axyridis over C. septempunctata are discussed.

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

Similar content being viewed by others

References

  • Agarwala, B. K., Yasuda, H., and Satoru, S. 2008. A life history response of a predatory ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) to food stress. Appl. Entomol. Zool. 43:183–189.

    Article  Google Scholar 

  • Altincicek, B., Gross, J., and Vilcinskas, A. 2008. Wounding-mediated gene expression and accelerated viviparous reproduction of the pea aphid Acyrthosiphon pisum. Insect Mol. Biol. 17:711–716.

    Article  CAS  PubMed  Google Scholar 

  • Boman, H. G., and Hultmark, D. 1987. Cell-free immunity in insects. Annu. Rev. Microbiol. 41:103–126.

    Article  CAS  PubMed  Google Scholar 

  • Brown, P.M.J., Adriaens, T., Bathon, H., Cuppen, J., Goldarazena, A., Hägg, T., Kenis, M., Klausnitzer, B.E.M., Kovář, I., Loomans, A.J.M., Majerus, M.E.N., Nedved, O., Pedersen, J., Rabitsch, W., Roy, H.E., Ternois, V., Zakharov, I.A., and Roy, D.B. 2008. Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. Biocontrol 53:5–21.

    Article  Google Scholar 

  • Brown, S.E., Howard, A., Kasparzak, A.B., Gordon, K.H., and East, P.D. 2009. A peptidomics study reveals the impressive antimicrobial peptide arsenal of the wax moth Galleria mellonella. Insect Biochem. Mol. Biol. 39:792–800.

    Article  CAS  PubMed  Google Scholar 

  • Bulet, P., and Stöcklin, R. 2005. Insect antimicrobial peptides: structures, properties and gene regulation. Prot. Peptide Letters 12:3–11.

    Article  CAS  Google Scholar 

  • Bulet, P., Cociancich, S., Dimarcq, J.-L., Lambert, J., Reichhart, J.-M., Hoffmann, D., Hetru, C., and Hoffmann, J.A. 1991. Isolation from a coleopteran insect of a novel inducible antibacterial peptide and of new members of the insect defensin family. J. Biol. Chem. 266:24520–24525.

    CAS  PubMed  Google Scholar 

  • Cai, L., Koziel, J. A., and O’neal, M. E. 2007. Determination of characteristic odorants from Harmonia axyridis beetles using in vivo solid-phase microextraction and multidimensional gas chromatography-mass spectrometry-olfactometry. J. Chromatogr. A 1147:66–78.

    Article  CAS  PubMed  Google Scholar 

  • Cottrell, T. E., and Shapiro-illan, D. I. (2003). Susceptibility of a native and an exotic lady beetle (Coleoptera: Coccinellidae) to Beauveria bassiana. J. Invertebr. Pathol. 84:137–144.

    Article  PubMed  Google Scholar 

  • Cottrell, T. E., and Shapiro-illan D. I. 2008. Susceptibility of endemic and exotic North American lady birds (Coleoptera: Coccinellidae) to endemic fungal entomopathogens. Eur. J. Entomol. 105:455–460.

    Google Scholar 

  • Declercq, P., Peeters, I., Vergauwe, G., and Thas. O. 2003. Interaction between Podisus maculiventris and Harmonia axyridis, two predators used in augmentative biological control in greenhouse crops. Biocontrol 48:39–55.

    Article  Google Scholar 

  • Fedorka, K. M., Zuk, M., and Mousseau, T. A. 2004. Immune suppression and the cost of reproduction in the ground cricket, Allonemobius socius. Evolution 58:2478–2485.

    PubMed  Google Scholar 

  • Gross, J., and Schmidtberg, H. 2009. Glands of leaf beetle larvae—protective structures against attacking predators and pathogens, pp. 177–178, in P. Jolivet, J. Santiago-Blay, and M. Schmidt (eds.). Research on Chrysomelidae, Vol. 2. Koninklijke Brill, Leiden, The Netherlands.

    Google Scholar 

  • Gross, J., Müller, C., Vilcinskas, A., and Hilker, M. 1998. Antimicrobial activity of the exocrine glandular secretions, haemolymph and larval regurgitate of the mustard leaf beetle Phaedon cochleariae. J. Invertebr. Pathol. 72:296–303.

    Article  PubMed  Google Scholar 

  • Gross, J., Podsiadlowski, L., and Hilker, M. 2002. Antimicrobial activity of the exocrine glandular secretions of Chrysomela larvae. J. Chem. Ecol. 28:317–331.

    Article  CAS  PubMed  Google Scholar 

  • Gross, J. Schumacher, K., Schmidtberg, H., and Vilcinskas, A. 2008. Protected by fumigants: beetle perfumes in antimicrobial defense. J. Chem. Ecol. 34:179–188.

    Article  CAS  PubMed  Google Scholar 

  • Gross, J., Kögel, S., and Hoffmann, C. 2010. Die Bedeutung des Asiatischen Marienkäfers Harmonia axyridis für den Obst- und Weinbau in Deutschland. Öko-Obstbau 1/2010:17–19.

    Google Scholar 

  • Hoang, A. 2001. Immune response to parasitism reduces resistance of Drosophila melanogaster to desiccation and starvation. Evolution 55:2353–2358.

    CAS  PubMed  Google Scholar 

  • Houg-goldstein, J., Cox, J., and Armstrong, A. 1996. Podisus maculiventris (Hemiptera: Pentatomidae) predation on ladybird beetles (Coleoptera: Coccinellidae). Fla. Entomol. 79:64–68.

    Article  Google Scholar 

  • Kamysz, W. and Turecka, K. 2005. Antimicrobial preservative effectiveness of natural peptide antibiotics. Acta Pol. Pharm. – Drug Res. 62:341–346.

    CAS  Google Scholar 

  • Koch, R. L. 2003. The multicolored 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 

  • Koch, R. L., and Galvan, T. L. 2008. Bad side of a good beetle: the North American experience with Harmonia axyridis. Biocontrol 53:23–35.

    Article  Google Scholar 

  • Koyama, S., and Majerus, M. E. N. 2008. Interactions between the parasitoid wasp Dinocampus coccinellae and two species of coccinellid from Japan and Britain. Biocontrol 53:253–264.

    Article  Google Scholar 

  • Krieg, A., Huger, A. M., Langenbruch, G. A., and Schnetter, W. 1984. New results on Bacillus thuringiensis var. tenebrionis with special regard to its effect on the Colorado beetle (Leptinotarsa decemlineata). J. Pest Sci. 57:145–150.

    Google Scholar 

  • Labrie, G., Lucas, E., and Coderre, D. 2006. Can developmental and behavioral characteristics of the multicolored Asian lady beetle Harmonia axyridis explain its invasive success? Biol. Invasions 8:743–754.

    Article  Google Scholar 

  • Lamberty, M., Ades, S., Uttenweiler-joseph, S., Brookhart, G., Bushey, D, Hoffmann, J. A., and Bulet, P. 1999. Isolation from the lepidopteran Heliothis virescens of a novel insect defensin with potent antifungal activity. J. Biol. Chem. 274:9320–9326.

    Article  CAS  PubMed  Google Scholar 

  • Lemaitre, B., Riechhart, J. M., and Hoffmann, J. A. 1997. Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc. Natl. Acad. Sci., USA 94:14614–14619.

    Article  CAS  PubMed  Google Scholar 

  • Marco, D. E., Paez, S. A., and Cannas, S. A. 2002. Species invasiveness in biological invasions: a modelling approach. Biol. Invasions 4:193–205.

    Article  Google Scholar 

  • Pell, J. K., Baverstock, J., Roy, H. E., Ware, R. L., and Majerus, M. E. M. 2008. Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. Biocontrol 53:147–168.

    Article  Google Scholar 

  • Pervez, A., and Omkar. 2006. Ecology and biological control application of multicoloured Asian ladybird, Harmonia axyridis: A review. Biocontr. Sci. Technol. 16:111–128.

    Article  Google Scholar 

  • Roy, H. E., and Wajnberg, E. 2008. From biological control to invasion: the ladybird Harmonia axyridis as a model species. Biocontrol 53:1–4.

    Article  Google Scholar 

  • Roy, H. E., Brown, P. M. J., Rothery, P., Ware, R. L., and Majerus, M. E. N. 2008. Interactions between the fungal pathogen Beauveria bassiana and three species of coccinellid: Harmonia axyridis, Coccinella septempunctata and Adalia bipunctata. Biocontrol 53:265–276.

    Article  Google Scholar 

  • Sachs, L. 1992. Angewandte Statistik, 7 Ed. Springer Verlag, Berlin.

    Google Scholar 

  • Schmid-hempel, P. 2005. Evolutionary ecology of insect immune defenses. Annu. Rev. Entomol. 50:529–551.

    Article  CAS  PubMed  Google Scholar 

  • Shapiro-ilan, D. I. and Cottrell, T. E. 2005. Susceptibility of lady beetles (Coleoptera: Coccinellidae) to entomopathogenic nematodes. J. Invertebr. Pathol. 89:150–156.

    Article  PubMed  Google Scholar 

  • Snyder, W. E., Clevenger, G. M., and Eigenbrode, S. D. 2004. Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia 140:559–565.

    Article  PubMed  Google Scholar 

  • Soares, A.O. and Serpa, A. 2007. Interference competition between ladybird beetle adults (Coleoptera: Coccinellidae): effects on growth and reproductive capacity. Popul. Ecol. 49:37–43.

    Article  Google Scholar 

  • Soares, A. O., Borges, I., Borges, P.A.V., Labrie, G., and Lucas, E. 2008. Harmonia axyridis: what will stop the invader? Biocontrol 53:127–145.

  • StatSoft I. 1999. STATISTICA for Windows users manual, version 5.5.

  • Stephen, W. P., and Johnson, O. W. 1962. Qualitative changes in insect blood after freezing. J. Kans. Entomol. Soc. 35:189–196.

    CAS  Google Scholar 

  • Vilcinskas, A. and Gross, J. 2005. Drugs from bugs: The use of insects as a valuable source of transgenes with potential in modern plant protection strategies. J. Pest Sci. 78:187–191.

    Article  Google Scholar 

  • Ware, R. L., and Majerus, M. E. N. 2008. Intraguild predation of immature stages of British and Japanese coccinellids by the invasive ladybird Harmonia axyridis. Biocontrol 53:169–188.

    Article  Google Scholar 

  • Yang, J., Yamamoto, M., Ishibashi, J., Taniai, K., and Yamakawa, M. 1998. Isolation, cDNA cloning and gene expression of an antibacterial protein from larvae of the coconut rhinoceros beetle, Oryctes rhinoceros. Eur. J. Biochem. 255:734–738.

    Article  CAS  PubMed  Google Scholar 

  • Yasuda, H., Evans, E. W., Kajita, Y., Urakawa, K., and Takizawa., T. 2004. Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia 141:722–731.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Svenja Hoferer, Jürgen Just, Vanessa Lessle, Kira Schneider, and Sabine Wetzel for excellent technical assistance. The authors thank Eva Gross for linguistic improvements and two anonymous reviewers for helpful comments on an earlier version of the manuscript.

Author information

Authors and Affiliations

  1. Julius Kühn Institute, Federal Research Centre for Cultivated Plants, Institute for Plant Protection in Fruit crops and Viticulture, Schwabenheimer Str. 101, 69221, Dossenheim, Germany

    Jürgen Gross, Astrid Eben, Ina Müller & Annette Wensing

  2. Departamento de Interacciones Multitroficas, Instituto de Ecología, A.C., Carretera Antigua a Coatepec No. 351, 91070, Xalapa, Veracruz, Mexico

    Astrid Eben

  3. School of Engineering and Science, Jacobs University Bremen, Campus Ring 1, 28759, Bremen, Germany

    Annette Wensing

Authors
  1. Jürgen Gross
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Astrid Eben
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ina Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Annette Wensing
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jürgen Gross.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gross, J., Eben, A., Müller, I. et al. A Well Protected Intruder: The Effective Antimicrobial Defense of the Invasive Ladybird Harmonia axyridis . J Chem Ecol 36, 1180–1188 (2010). https://doi.org/10.1007/s10886-010-9867-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-010-9867-2

Key Words

Search

Navigation