BioControl

, Volume 53, Issue 1, pp 89–102

Phenotypic variation in invasive and biocontrol populations of the harlequin ladybird, Harmonia axyridis

  • Eric Lombaert
  • Thibaut Malausa
  • Rémi Devred
  • Arnaud Estoup
Article

Abstract

Despite numerous releases for biological control purposes during more than 20 years in Europe, Harmonia axyridis failed to become established until the beginning of the 21st century. Its status as invasive alien species is now widely recognised. Theory suggests that invasive populations should evolve toward greater phenotypic plasticity because they encounter differing environments during the invasion process. On the contrary, populations used for biological control have been maintained under artificial rearing conditions for many generations; they are hence expected to become specialised on a narrow range of environments and show lower phenotypic plasticity. Here we compared phenotypic traits and the extent of adaptive phenotypic plasticity in two invasive populations and two populations commercialized for biological control by (i) measuring six phenotypic traits related to fitness (eggs hatching rate, larval survival rate, development time, sex ratio, fecundity over 6 weeks and survival time of starving adults) at three temperatures (18, 24 and 30°C), (ii) recording the survival rate and quiescence aggregation behaviour when exposed to low temperatures (5, 10 and 15°C), and (iii) studying the cannibalistic behaviour of populations in the absence of food. Invasive and biocontrol populations displayed significantly different responses to temperature variation for a composite fitness index computed from the traits measured at 18, 24 and 30°C, but not for any of those traits considered independently. The plasticity measured on the same fitness index was higher in the two invasive populations, but this difference was not statistically significant. On the other hand, invasive populations displayed significantly higher survival and higher phenotypic plasticity when entering into quiescence at low temperatures. In addition, one invasive population displayed a singular cannibalistic behaviour. Our results hence only partly support the expectation of increased adaptive phenotypic plasticity of European invasive populations of H. axyridis, and stress the importance of the choice of the environmental parameters to be manipulated for assessing phenotypic plasticity variation among populations.

Keywords

Adaptive phenotypic plasticity Alien species Biological control Harmonia axyridis Biological invasion 

References

  1. Agarwala BK, Dixon AFG (1993) Kin recognition: egg and larval cannibalism in Adalia bipunctata (Coleoptera: Coccinellidae). Eur J Entomol 90:45–50Google Scholar
  2. Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326CrossRefPubMedGoogle Scholar
  3. Berkvens N, Bonte J, Berkvens D, Deforce K, Tirry L, De Clercq P (2007) Pollen as an alternative food for Harmonia axyridis. BioControl (this issue). doi:10.1007/s10526-007-9128-7
  4. Brown PMJ, Adriaens T, Bathon H, Cuppen J, Goldarazena A, Hägg T, Kenis M, Klausnitzer BEM, Kovář I, Loomans AJM, Majerus MEN, Nedved O, Pedersen J, Rabitsch W, Roy HE, Ternois V, Zakharov IA, Roy DB (2007a) Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl (this issue). doi:10.1007/s10526-007-9132-y
  5. Brown PMJ, Roy HE, Rothery P, Roy DB, Ware RL, Majerus MEN (2007b) Harmonia axyridis in the Great Britain: analysis of the spread and distribution of a non-native coccinellid. BioControl (this issue). doi:10.1007/s10526-007-9124-y
  6. Coutanceau J-P (2006) Harmonia axyridis (Pallas, 1773): une Coccinelle asiatique introduite, acclimatée et en extension en France. Bulletin de la société entomologique de France 111:395–401Google Scholar
  7. Debat V, David P (2001) Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol Evol 16:555–561CrossRefGoogle Scholar
  8. Geng YP, Pan XY, Xu CY, Zhang WJ, Li B, Chen JK, Lu BR, Song ZP (2007) Phenotypic plasticity rather than locally adapted ecotypes allows the invasive alligator weed to colonize a wide range of habitats. Biol Invasions 9:245–256CrossRefGoogle Scholar
  9. Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407CrossRefGoogle Scholar
  10. Grill CP, Moore AJ, Brodie ED (1997) The genetics of phenotypic plasticity in a colonizing population of the ladybird beetle, Harmonia axyridis. Heredity 78:261–269Google Scholar
  11. Kaufman SR, Smouse PE (2001) Comparing indigenous and introduced populations of Melaleuca quinquenervia (Cav.) Blake: response of seedlings to water and pH levels. Oecologia 127:487–494CrossRefGoogle Scholar
  12. Koch RL (2003) The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J Insect Sci 3:1–16CrossRefGoogle Scholar
  13. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16:199–204CrossRefPubMedGoogle Scholar
  14. Lambrinos JG (2004) How interactions between ecology and evolution influence contemporary invasion dynamics. Ecology 85:2061–2070CrossRefGoogle Scholar
  15. Lee CE, Remfert JL, Chang YM (2007) Response to selection and evolvability of invasive populations. Genetica 129:179–192CrossRefPubMedGoogle Scholar
  16. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  17. Majerus MEN, Strawson V, Roy H (2006) The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecol Entomol 31:207–215CrossRefGoogle Scholar
  18. Malausa T, Guillemaud T, Lapchin L (2005) Combining genetic variation and phenotypic plasticity in tradeoff modelling. Oikos 110:330–338CrossRefGoogle Scholar
  19. Masel J, King OD, Maughan H (2007) The loss of adaptive plasticity during long periods of environmental stasis. Am Nat 169:38–46CrossRefPubMedGoogle Scholar
  20. Osawa N (1992) Sibling cannibalism in the ladybird beetle Harmonia axyridis: fitness consequences for mother and offspring. Res Popul Ecol 34:45–55CrossRefGoogle Scholar
  21. Pervez A, Gupta AK, Omkar (2005) Kin recognition and avoidance of kin cannibalism by the larvae of co-occurring ladybirds: a laboratory study. Eur J Entomol 102:513–518Google Scholar
  22. Pervez A, Gupta AK, Omkar (2006) Larval cannibalism in aphidophagous ladybirds: influencing factors, benefits and costs. Biol Control 38:307–313CrossRefGoogle Scholar
  23. Polis GA (1981) The evolution and dynamics of intraspecific predation. Annu Rev Ecol Syst 12:225–251CrossRefGoogle Scholar
  24. Preziosi RF, Snyder WE, Grill CP, Moore AJ (1999) The fitness of manipulating phenotypes: implications for studies of fluctuating asymmetry and multivariate selection. Evolution 53:1312–1318CrossRefGoogle Scholar
  25. Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993CrossRefPubMedGoogle Scholar
  26. 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 (in press)Google Scholar
  27. SAS Institute Inc. (1999) SAS/Stat user’s guide, version 8. SAS Institute, CaryGoogle Scholar
  28. Schanderl H, Ferran A, Garcia V (1988) Rearing two coccinellids Harmonia axyridis and Semiadalia undecimnotata on eggs of Anagasta kuehniella killed with ultraviolet radiation. Entomol Exp Appl 49:235–244CrossRefGoogle Scholar
  29. Scheiner SM (1993) Genetics and evolution of phenotypic plasticity. Annu Rev Ecol Syst 24:35–68CrossRefGoogle Scholar
  30. Specty O, Febvay G, Grenier S, Delobel B, Piotte C, Pageaux JF, Ferran A, Guillaud J (2003) Nutritional plasticity of the predatory ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae): comparison between natural and substitution prey. Arch Insect Biochem Physiol 52:81–91CrossRefPubMedGoogle Scholar
  31. Stillwell R, Wallin W, Hitchcock L, Fox C (2007) Phenotypic plasticity in a complex world: interactive effects of food and temperature on fitness components of a seed beetle. Oecologia 153:309–321CrossRefPubMedGoogle Scholar
  32. Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends Ecol Evol 18:94–101CrossRefGoogle Scholar
  33. Tourniaire R, Ferran A, Gambier J, Giuge L, Bouffault F (2000a) Locomotory behavior of flightless Harmonia axyridis pallas (Col., Coccinellidae). J Insect Physiol 46:721–726CrossRefPubMedGoogle Scholar
  34. Tourniaire R, Ferran A, Giuge L, Piotte C, Gambier J (2000b) A natural flightless mutation in the ladybird, Harmonia axyridis. Entomol Exp Appl 96:33–38CrossRefGoogle Scholar
  35. Valladares F, Sanchez Gomez D, Zavala MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J Ecol 94:1103–1116CrossRefGoogle Scholar
  36. van Lenteren JC, Loomans AJM, Babendreier D, Bigler F (2007) Harmonia axyridis: an environmental risk assessment for Northwest Europe. BioControl (this issue). doi:10.1007/s10526-007-9120-2
  37. Williams T, Hernandez O (2006) Costs of cannibalism in the presence of an iridovirus pathogen of Spodoptera frugiperda. Ecol Entomol 31:106–113CrossRefGoogle Scholar
  38. Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666CrossRefGoogle Scholar
  39. Yeh PJ, Price TD (2004) Adaptive phenotypic plasticity and the successful colonization of a novel environment. Am Nat 164:531–542CrossRefPubMedGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2007

Authors and Affiliations

  • Eric Lombaert
    • 1
  • Thibaut Malausa
    • 2
  • Rémi Devred
    • 2
  • Arnaud Estoup
    • 3
  1. 1.Centre de Recherches de Sophia Antipolis, Unité de Lutte BiologiqueINRASophia Antipolis CedexFrance
  2. 2.INRA, UMR ROSE (INRA/UNSA)Sophia-Antipolis CedexFrance
  3. 3.INRA, UMR CBGP (INRA/IRD/Cirad/Montpellier SupAgro)Montferrier-sur-Lez CedexFrance

Personalised recommendations