Skip to main content
SpringerLink
Log in

Influence of Diet on Fecundity, Immune Defense and Content of 2-Isopropyl-3-Methoxypyrazine in Harmonia axyridis Pallas

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

Abstract

Food type can affect all functional aspects of an insect’s life. We investigated the effects of different diet regimes on life history parameters of the ladybird beetle Harmonia axyridis. Furthermore, we tested the importance of elytral color, sex, and diet on chemical and immune defense in this species. We also compared hemolymph from cohorts of H. axyridis and Coccinella septempunctata (Coleoptera: Coccinellidae) fed different diets to examine effects on the 2-isopropyl-3-methoxypyrazine (IPMP) content in these beetles. No effects of diet on the duration of larval development and on adult weight were found. We detected, however, significantly higher fecundity and oviposition rates when female H. axyridis were reared on pea aphids than when reared on eggs of Ephestia kuehniella. Males and females did not differ in their immune response. Elytral color affected both immune defense and chemical defense. The antimicrobial activity of the hemolymph differed only when morphotypes were tested against E. coli. Moreover, we observed an effect of elytral pigmentation on IPMP content. The succinea 2 type (orange without dots) had the lowest IPMP content in two out of three feeding regimes compared to the succinea 1 (orange with dots) type. Depending on diet, IPMP contents differed in both species leading to higher contents either in H. axyridis or C. septempunctata. Furthermore, aphid species ingested during larval development significantly affected IPMP content in adult beetles. These results implicate new aspects for risk assessment of H. axyridis in viticulture.

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

  • Al Abassi, S., Birkett, M. A., Pettersson, J., Pickett, J. A., and Woodcock, C. M. 1998. Ladybird beetle odour identified and found to be responsible for attraction between adults. Cell. Mol. Life Sci. 54:876–879.

    Article  CAS  Google Scholar 

  • Alhmedi, A., Haubruge, E., and Francis, F. 2008. Role of prey-host associations on Harmonia axyridis and Episyrphus balteatus reproduction and predatory efficiency. Entomol. Exp. Appl. 128:49–56.

    Article  Google Scholar 

  • Alyokhin, A. and Francis, F. 2005. Density-dependent regulation in populations of potato-colonizing aphids. Popul. Ecol. 47:257–266.

    Article  Google Scholar 

  • Amaral, J. S., Valentão, P., Andrade, P. B., Martins, R. C., and Seabra, R. M. 2010. Phenolic composition of hazelnut leaves: Influence of cultivar, geographical origin and ripening stage. Sci. Hortic. 126:306–313.

    Article  CAS  Google Scholar 

  • Armitage, S. A. O., Thompson, J. J. W., Rolff, J., and Siva-Jothy, M. T. 2003. Examining costs of induced and constitutive immune investment in Tenebrio molitor. J. Evol. Biol. 16:1038–1044.

    Article  PubMed  CAS  Google Scholar 

  • Barnes, A. I. and Siva-Jothy, M. T. 2000. Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanization is an indicator of investment in immunity. Proc. R. Soc. Lond. B 267:177–182.

    Article  CAS  Google Scholar 

  • Berkvens, N., Bonte, J., Berkvens, D., Tirry, L., and De Clercq, P. 2008. Influence of diet and photoperiod on development and reproduction of European populations of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). BioControl 53:211–221.

    Article  Google Scholar 

  • Bezzerides, A. L., Mcgraw, K. J., Parker, R. S., and Husseini, J. 2007. Elytral color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis. Behav. Ecol. Sociobiol. 61:1401–1408.

    Article  Google Scholar 

  • Botezatu, A. and Pickering, G. J. 2010. Ladybug (Coccinellidae) taint in wine, in A. G. Reynolds (ed.), Understanding and Managing Wine Quality and Safety. Woodhead Publishing Limited, Cambridge.

    Google Scholar 

  • Bulet, P., Cocianicich, 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.

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Carton, Y. and Nappi, A. J. 1997. Drosophila cellular immunity against parasitoids. Parasitol. Today 13:218–227.

    Article  PubMed  CAS  Google Scholar 

  • Cudjoe, E., Wiederkehr, T. B., and Brindle, I. D. 2005. Headspace gas chromatography–mass spectrometry: a fast approach to the identification and determination of 2-alkyl-3-methoxypyrazine pheromones in ladybugs. Analyst 130:152–155.

    Article  PubMed  CAS  Google Scholar 

  • D’Abrosca, B., Dellagreca, M., Fiorentino, A., Monaco, P., Previtera, L., Simonet, A. M., and Zarelli, A. 2011. Potential allelochemicals from Sambucus nigra. Phytochemistry 58:1073–1081.

    Article  Google Scholar 

  • De Jong, P. W. and Brakefield, P. M. 1998. Climate and change in clines for melanism in the two-dot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). Proc. Roy. Soc. Lond. B. Biol. Sci. 265:39–43.

    Article  Google Scholar 

  • De jong, P. W., Gussekloo, S. W. S., and Brakefield, P. M. 1996. Differences in thermal balance, body temperature and activity between non melanic and melanic two-dot laybird beetles (Adalia bipunctata) under controlled conditions. J. Exp. Biol. 199:2655–2666.

    Google Scholar 

  • Deutsches Institut Für Normung. 2010. DIN 58940: Susceptibility testing of pathogens to antimicrobial agents—Part 4: Evaluation classes of the minimum inhibitory concentration, pp. 354–60, in DIN-Taschenbuch Medizinische Mikrobiologie und Immunologie, Normen und weitere Unterlagen. Beuth-Verlag, Berlin and Cologne.

  • Ferran, A., Niknam, H., Kabiri, F., Picart, J. L., Deherve, C., Brun, J., Iperti, G., and Lapchin, L. 1996. The use of Harmonia axyridis larvae (Coleoptera: Coccinellidae) against Macrosiphum rosae (Hemiptera: Sternorrhyncha: Aphididae) on rose bushes. Eur. J. Entomol. 93:59–67.

    Google Scholar 

  • Finlayson, C., Alyokhin A., Gross S., and Porter E. 2010. Differential consumption of four aphid species by four lady beetle species. J. Insect Sc. 10:10:31 available online: insectscience.org/10.31.

  • Francis, F., Haubrige, E., and Gaspar, C. 2000. Influence of host plants on specialist/generalist aphids and on the development of Adalia bipunctata (Coleoptera: Coccinellidae). Eur. J. Entomol. 97:481–485.

    CAS  Google Scholar 

  • Fukunaga, Y. and Akimoto, S. 2007. Toxicity of the aphid Aulacorthum magnolia to the predator Harmonia axyridis (Coeloptera: Coccinellidae) and genetic variance in the assimiliation of the toxic aphids in H. axyridis larvae. Entomol. Sci. 10:45–53.

    Article  Google Scholar 

  • Galvan, T. L., Burkness, E. C., Vickers, Z., Stenberg, P., Mansfield, A. K., and Hutchison, W. D. 2007. Sensory-based action threshold for multicolored Asian lady beetle-related taint in winegrapes. Am. J. Enol. Viticult. 58:518–522.

    Google Scholar 

  • Galvan, T. L., Koch, R. L., and Hutchinson, W. D. 2008. Impact of fruit feeding on overwintering survival of the multicolored Asian lady beetle, and the ability of this insect and paper wasps to injure wine grape berries. Entomol. Exp. Appl. 128:429–436.

    Article  Google Scholar 

  • Grill, C. P. and Moore, A. J. 1998. Effects of a larval antipredator response and larval diet on adult phenotype in an aposematic ladybird beetle. Oecologia 114:274–282.

    Article  Google Scholar 

  • Gross, J., Fatouros, N. E., and Hilker, M. 2004a. The significance of bottom-up effects for host plant specialization in Chrysomela leaf beetles. Oikos 105:368–376.

    Article  Google Scholar 

  • Gross, J., Schmolz, E., and Hilker, M. 2004b. Thermal adaptations of the leaf beetle Chrysomela lapponica to different climes of Central and Northern Europe. Environ. Entomol. 33:799–806.

    Article  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  PubMed  CAS  Google Scholar 

  • Gross, J., Eben, A., Müller, I., and Wensing, A. 2010. A well protected intruder: the effective antimicrobial defense of the invasive ladybird Harmonia axyridis. J. Chem. Ecol. 36:1180–1188.

    Article  PubMed  CAS  Google Scholar 

  • Haine, E. R., Moret, Y., Siva-Jothy, M. T., and Rolff, J. 2008. Antimicrobial defense and persistent infection in insects. Science 322:1257–1259.

    Article  PubMed  CAS  Google Scholar 

  • Hodek, I. 1993. Habitat and food specificity in aphidophagous predators. Biocontr. Sci. Technol. 3:91–100.

    Article  Google Scholar 

  • Hodek, I. and Honek, A. 1996. Ecology of Coccinellidae. Kluwer, Dordrecht. 464.

    Google Scholar 

  • Hukusima, S. and Kamei, M. 1970. Effects of various species of aphids as food on development, fecundity and longevity of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Res. Bull. Fac. Agric. Gifu Univ. 29:53–66.

    Google Scholar 

  • Jalali, M. A., Tirry, L., and De Clercq, P. 2009. Effects of food and temperature on development, fecundity and life-table parameters of Adalia bipunctata (Coleoptera: Coccinellidae). J. Appl. Entomol. 133:615–625.

    Article  Google Scholar 

  • Kalushkov, P. and Hodek, I. 2004. The effects of thirteen species of aphids on some life history parameters of the ladybird Coccinella septempunctata. Biocontrol 49:21–32.

    Article  Google Scholar 

  • Karl, I., Hoffmann, K. H., and Fischer, K. 2010. Cuticular melanisation and immune response in a butterfly: local adaptation and lack of correlation. Ecol. Ent. 35:523–528.

    Google Scholar 

  • Kindlmann, P., Ameixa, O. M. C. C., and Diyon, A. F. G. 2011. Ecological effects of invasive alien species on native communities, with particular emphasis on the interactions between aphids and ladybirds. Biocontrol 56:469–476.

    Article  Google Scholar 

  • Klausnitzer, B. and Klausnitzer H. 1997. Marienkäfer: Westarp Wissenschaften.

  • 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. 3:32–48.

    PubMed  CAS  Google Scholar 

  • Kögel, S., Gross, J., and Hoffmann, C. 2012a. Sensory detection thresholds of ‘ladybird taint’ in ‘Riesling’ and ‘Pinot noir’ under different fermentation and processing conditions. Vitis 51:27–32.

    Google Scholar 

  • Kögel, S., Gross, J., Hoffmann, C., and Ulrich, D. 2012b. Diversity and frequencies of methoxypyrazines in hemolymph of Harmonia axyridis and Coccinella septempunctata and their influence on the taste of wine. Eur. Food Res. Technol. 234:399–404.

    Article  Google Scholar 

  • Lanzoni, A., Accinelli, G., Bazzocchi, G. G., and Burgio, G. 2004. Biological traits and life table of the exotic Harmonia axyridis compared with Hippodamia variegata, and Adalia bipunctata (Coleoptera: Coccinellidae). J. Appl. Entomol. 28:298–306.

    Article  Google Scholar 

  • Lee, K. P., Simpson, S. J., and Wilson, K. 2008. Dietary protein-quality influences melanization and immune function in an insect. Funct. Ecol. 22:1052–1061.

    Article  Google Scholar 

  • Mcclure, M. S. 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 

  • Michie, L. J., Mallard, F., Majerus, M. E. N., and Jiggins, F. M. 2010. Melanic through nature or nurture: genetic polymorphism and phenotypic plasticity in Harmonia axyridis. J. Evol. Biol. 27:1699–1707.

    Article  Google Scholar 

  • Moore, B. P. and Brown, W. V. 1981. Identification of warning odour components, bitter principles and antifeedants in an aposematic beetle: Metriorrhynchus rhipidius (Coleoptera: Lycicae). Insect Biochem. 11:493–499.

    Article  CAS  Google Scholar 

  • Nedved, O. and Salvucci, S. 2008. Ladybird Coccinella septempunctata (Coleoptera: Coccinellidae) prefers toxic prey in laboratory choice experiment. Eur. J. Entomol. 105:431–436.

    Google Scholar 

  • Osawa, N. 1993. Population field studies of the aphidophagous ladybird beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae): life tables and key factor analysis. Res. Popul. Ecol. 35:335–348.

    Article  Google Scholar 

  • Osawa, N. and Nishida, T. 1992. Seasonal variation in elytral colour polymorphism in Harmonia axyridis (the ladybird beetle): the role on non-random mating. Heredity 69:297–307.

    Article  Google Scholar 

  • Patton, C. A., Ranney, T. G., Burton, J. D., and Walgenbach, J. F. 1997. Natural pest resistance of Prunus taxa to feeding by adult Japanese Beetles: role of endogenous allelochemicals in host plant resistance. J. Am. Soc. Hort. Sci. 122(5):668–672.

    Google Scholar 

  • Pickering, G. J., Lin, J., Riesen, R., Reynolds, A., Brindle, I., and Soleas, G. 2004. Influence of Harmonia axyridis on the sensory properties of white and red wine. Am. J. Enol. Viticult. 55:153–159.

    Google Scholar 

  • Pickering, G. J., Lin, Y., Reynolds, A., Soleas, G., Riesen, R., and Brindle, I. 2005. The influence of Harmonia axyridis on wine composition and aging. J. Food Sci. 70:128–135.

    Article  Google Scholar 

  • Ross, C. F., Rosales, M. U., and Fernandez-Plotka, V. C. 2010. Aroma profile of Niagara grape juice contaminated with multicoloured Asian lady beetle taint using gas chromatography/mass spectrometry/olfactometry. Int. J. Food Sci. Technol. 45:789–793.

    Article  CAS  Google Scholar 

  • Rothschild, M. 1961. Defensive odours and Muellerian mimicry among insects. Trans. Roy. Ent. Soc. Lond. 113:101–121.

    Article  Google Scholar 

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

    Google Scholar 

  • Seo, M. J., Kim, G. H., and Youn, Y. N. 2008. Differences in biological and behavioural characteristics of Harmonia axyridis (Coleoptera: Coccinellidae) according to colour patterns of elytra. J. Appl. Entomol. 132:239–247.

    Article  Google Scholar 

  • Sloggett, J. J. 2010. Colour pattern polymorphism and chemical defence in Harmonia axyridis. IOBC/wprs Bulletin 58:114–123.

    Google Scholar 

  • Snyder, W. E., Joseph, S. B., Preziosi, R. F., and Moore, A. J. 2000. Nutritional benefits of cannibalism for the lady beetle Harmonia axyridis (Coleoptera: Coccinellidae) when prey quality is poor. Environ. Ent. 29:1173–1179.

    Article  Google Scholar 

  • Soares, A. O., Coderre, D., and Schanderl, H. 2001. Fitness of two phenotypes of Harmonia axyridis (Coleoptera: coccinellidae). Eur. J. Entomol. 98:287–293.

    Google Scholar 

  • Soares, A. O., Coderre, D., and Schanderl, H. 2003. Effect of temperature and intraspecific allometry on predation by two phenotypes of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Environ. Entomol. 32:939–944.

    Article  Google Scholar 

  • Soares, A. O., Coderre, D., and Schanderl, H. 2004. Dietary self-selection behaviour by the adults of the aphidophagous ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae) J. Animal Ecol. 73:478–486.

    Article  Google Scholar 

  • Soares, A. O., Coderre, D., and Schanderl, H. 2005. Influence of prey quality in the finess of two phenotypes of Harmonia axyridis adults. Ent. Exp. Appl. 114:227–232.

    Article  Google Scholar 

  • Specty, O., Febvay, G., Grenier, S., Delober, B., Piotte, C., Pageaux, J. F., Ferran, A., and Guillaud, J. 2003. Nutritional plasticity of the predatory ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae): comparison between natural and substitution prey. Arch. Insect Biochem. Physiol. 52:81–91.

    Article  PubMed  CAS  Google Scholar 

  • Stathas, G. J., Eliopoulos, P. A., Kontodimas, D. C., and Giannopapas, J. 2001. Parameters of reproductive activity in females of Harmonia axyridis. Eur. J. Entomol. 98:547–549.

    Google Scholar 

  • Su, W., Michaud, J. P., Runzhi, Z., Fan, Z., and Shuang, L. 2009. Seasonal cycles of assortative mating and reproductive behaviour in polymorphic populations of Harmonia axyridis in China. Ecol. Entomol. 34:483–494.

    Article  Google Scholar 

  • Tedders, W. L. and Schaefer, P. 1994. Release and establishment of Harmonia axyridis (Coleoptera, Coccinellidae) in the southeastern United-States. Entomol. News 105:228–243.

    Google Scholar 

  • Ungerova, D., Kalushkov, P., and Nedved, O. 2010. Suitability of diverse prey species for development of Harmonia axyridis and the effect of container size. IOBC/wprs Bulletin 58:165–174.

    Google Scholar 

  • Wilson, K., Cotter, S. C., Reeson, A. F., and Pell, J. K. 2001. Melanism and disease resistance in insects. Ecol. Lett. 4:637–649.

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the ‘Forschungsring Deutscher Weinbau’ (FDW). The authors thank Svenja Hoferer and Sabine Wetzel (JKI Dossenheim) for technical assistance. We thank the Norddeutsche Pflanzenzucht KG for a gift of untreated seeds of Vicia fabae (cultivar “Tattoo”). We are grateful to M. Paulus and C. Emmerling from FB VI Geography/Biogeography, Trier University (Germany) for cooperation. Special thanks go to Th. Thieme (BioTest Labor, Sagerheide, Germany) who provided expertise on the determination of field collected aphid species, and Eva Gross (Dossenheim, Germany) and Lukasz Stelinski (Lake Alfred, Florida, USA) for linguistic improvements.

Author information

Authors and Affiliations

  1. Julius Kühn-Institut, Federal Research Center for Cultivated Plants, Institute for Plant Protection in Fruit Crops and Viticulture, Geilweilerhof, 76833, Siebeldingen, Germany

    Susanne Kögel & Christoph Hoffmann

  2. Julius Kühn-Institut, Federal Research Center for Cultivated Plants, Institute for Plant Protection in Fruit Crops and Viticulture, Schwabenheimer Str. 101, 69221, Dossenheim, Germany

    Astrid Eben & Jürgen Gross

Authors
  1. Susanne Kögel
    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. Christoph Hoffmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jürgen Gross
    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

Kögel, S., Eben, A., Hoffmann, C. et al. Influence of Diet on Fecundity, Immune Defense and Content of 2-Isopropyl-3-Methoxypyrazine in Harmonia axyridis Pallas. J Chem Ecol 38, 854–864 (2012). https://doi.org/10.1007/s10886-012-0139-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-012-0139-1

Keywords

Search

Navigation