Biological Invasions

, Volume 21, Issue 2, pp 519–529 | Cite as

Comparative functional responses of introduced and native ladybird beetles track ecological impact through predation and competition

  • Steven CrookesEmail author
  • Emma M. DeRoy
  • Jaimie T. A. Dick
  • Hugh J. MacIsaac
Original Paper


Recent advances in invasion research has highlighted that differences in the feeding ecology of native and non-native species manifest through differences in their functional responses (FRs) and that FRs track ecological impact. Further, as with plant competition studies, differential resource use patterns may illuminate competition mechanisms among animal taxa. Ladybirds are a diverse family of beetles that possess substantial variation in body mass across taxa. Further, some ladybird species have been widely introduced into novel habitats, where they may pose significant risks of ecological and economic harm. By controlling for allometric scaling, we tested the hypothesis that introduced Asian multicoloured ladybirds (Harmonia axyridis) are more efficient predators on aphids than trophically-analogous, native convergent ladybirds (Hippodamia convergens). We utilized a prey-replacement FR design, and assessed rates of pea aphid consumption as a function of initial prey density. H. axyridis possessed significantly higher absolute and mass-adjusted FRs (Type II) than the native species, consistent with expectations. The higher FR was mediated by reduced handling time, suggesting that the ability of H. axyridis to manipulate and digest prey exceeds that of H. convergens. Our feeding results may explain, in part, the increasing occurrence and abundance of the introduced species, and documented declines of native species of prey and competitor in invaded habitats.


Functional response Invasion Non-indigenous species Limiting similarity Niche Sympatry 



We thank Drs. Dan Pritchard and Steven Marshall for analytical and field advice and Dr. Trevor Pitcher with experimental setup and execution. We are also indebted to the comments made by two referees that enhanced the manuscript. We are grateful for funding from an NSERC Discovery Grant and Canada Research Chair to HJM.


  1. Acar EB, Medina JC, Lee ML, Booth GM (2001) Olfactory behaviour of convergent lady beetle (Coleoptera: Coccinellidae) to alarm pheromone of green peach aphid (Hemiptera: Aphididae). Can J Entomol 133:389–397CrossRefGoogle Scholar
  2. Acar EB, Mill DD, Smith BN, Hansen LD, Booth GM (2005) Comparison of respiration in adult Harmonia axyridis (Pallas) and Hippodamia convergens Guerrin-Manaville (Coleoptera: Coccinellidae). Environ Entomol 34:241–245CrossRefGoogle Scholar
  3. Alexander ME, Dick JTA, Weyl OLF, Robinson TB, Richardson DM (2014) Existing and emerging high impact invasive species are characterised by higher functional responses than natives. Biol Lett 10(2):20130946. CrossRefGoogle Scholar
  4. Coderre D, Lucas E, Gagné I (1995) The occurrence of Harmonia axyridis (Pallas) (Coleptera: Coccinellidae) in Canada. Can Entomol 127:609–611CrossRefGoogle Scholar
  5. Dick JTA, Alexander ME, Jeschke JM, Ricciardi A, MacIsaac HJ, Robinson TB, Kumschick S, Weyl OLF, Dunn AM, Hatcher MJ, Paterson RA, Farnsworth KD, Richardson DM (2014) Advancing impact prediction and hypothesis testing in invasion ecology using a comparative functional response approach. Biol Invasions 16:735–753CrossRefGoogle Scholar
  6. Dick JTA, Laverty C, Lennon JJ, Barrios-O’Neill D, Mensink PJ, Britton JR, Medoc V, Boets P, Alexander ME, Taylor NG, Dunn AM, Hatcher MJ, Rosewarne PJ, Crookes S, MacIsaac HJ, Xu M, Ricciardi A, Wasserman RJ, Ellender BR, Weyl OLF, Lucy FE, Banks PB, Dodd JA, MacNeil C, Penk MR, Aldridge DC, Caffrey JM (2017) Invader relative impact potential: a new metric to understand and predict the ecological impacts of existing, emerging and future invasive alien species. J Appl Ecol 54:1259–1267CrossRefGoogle Scholar
  7. Dixon AFG, Hemptinne J-L (2001) Body size distribution in predatory ladybird beetles reflects that of their prey. Ecology 82:1847–1856CrossRefGoogle Scholar
  8. Dreistadt SH, Flint ML (1996) Melon aphid (Homoptera: Aphididae) control by inundative convergent lady beetle (Coleoptera: Coccinellidae) release on chrysanthemum. Environ Entomol 25:688–697CrossRefGoogle Scholar
  9. Elton CS (1958) The ecology of invasions by animals and plants. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  10. Emery SM (2007) Limiting similarity between invaders and dominant species in herbaceous plant communities? J Ecol 95:1027–1035CrossRefGoogle Scholar
  11. Gordon RD (1985) The Coleoptera (Coccinellidae) of America north of Mexico. J N Y Entomol Soc 93:1–912Google Scholar
  12. Hassell M, Lawton J, Beddington J (1977) Sigmoid functional responses by invertebrate predators and parasitoids. J Anim Ecol 46:249–262CrossRefGoogle Scholar
  13. Hesler SL, McNickle G, Catangui MA, Losey JE, Beckendorf EA, Stellwag L, Brandt DM, Bartlett PB (2012) Method for continuously rearing Coccinella lady beetles (Coleoptera: Coccinellidae). Open Entomol J 6:42–46CrossRefGoogle Scholar
  14. Hinkleman TM, Tenhumberg B (2013) Larval performance and kill rate of convergent ladybird beetles, Hippodamia convergens, on black bean aphids, Aphis fabae, and pea aphids, Acyrthosiphon pisum. J Insect Sci 13:46Google Scholar
  15. Hoebeke ER, Wheeler AG (1996) Adventive lady beetles (Coleoptera: Coccinellidae) in the Canadian Maritime provinces, with new eastern U.S. records of Harmonia quadripunctata. Entomol News 107:281–290Google Scholar
  16. Holling CS (1959) The components of predation as revealed by a study of small mammal predation of the European sawfly. Can Entomol 91:298–385Google Scholar
  17. Ingels B, van Hassel P, van Leeuwen T, de Clercq P (2015) Feeding history affects intraguild interactions between Harmonia axyridis (Coleoptera: Coccinellidae) and Episyrphus balteatus (Diptera: Syrphidae). PLoS ONE. Google Scholar
  18. Jeschke JM, Kopp M, Tollrian R (2002) Predator functional responses: discriminating between handling and digesting prey. Ecol Monogr 72:95–112CrossRefGoogle Scholar
  19. Juliano SA (2001) Nonlinear curve-fitting: predation and functional response curves. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, Oxford, pp 178–196Google Scholar
  20. Kalinkat G, Schneider FD, Digel C, Guill C, Rall BC, Brose U (2013) Body masses, functional responses and predator-prey stability. Ecol Lett 16:1126–1134CrossRefGoogle Scholar
  21. Klecka J, Boukal DS (2013) Foraging and vulnerability traits modify predator-prey body mass allometry: freshwater macroinvertebrates as a case study. J Anim Ecol 82:1031–1041CrossRefGoogle Scholar
  22. Kleiber M (1932) Body size and metabolism. Hilgardia 6:315–353CrossRefGoogle Scholar
  23. Lamana ML, Miller JC (1998) Temperature-dependent development in an Oregon population of Harmonia axyridis (Coleoptera: Coccinellidae). Environ Entomol 27:1001–1005CrossRefGoogle Scholar
  24. Lamb RJ, MacKay PA, Gerber GH (1987) Are development and growth of pea aphids, Acyrthosiphon pisum, in North America adapted to local temperatures? Oecologia 72:170–177CrossRefGoogle Scholar
  25. Lawton JH, Brown KC (1986) The population and community ecology of invading insects. Philos Trans R Soc Lond B 314:607–616CrossRefGoogle Scholar
  26. Lawton JH, Hassell MP (1981) Asymmetrical competition in insects. Nature 289:793–795CrossRefGoogle Scholar
  27. Lee J-H, Kang T-J (2004) Functional response of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) to Aphis gossypii Glover (Homoptera; Aphididae) in the laboratory. Biol Control 31:306–310CrossRefGoogle Scholar
  28. Lenski RE (1984) Food limitation and competition: a field experiment with two Carabus species. J Anim Ecol 53:203–216CrossRefGoogle Scholar
  29. Matzek V (2012) Trait values, not trait plasticity, best explain invasive species’ performance in a changing environment. PLoS ONE. Google Scholar
  30. Minelli A, Pasqual C (1977) The mouthparts of ladybirds: structure and function. Bolletino di Zool 44:183–187CrossRefGoogle Scholar
  31. Murdoch WW (1983) The functional response of predators. J Appl Ecol 10:335–342Google Scholar
  32. Poling TD, Hayslette SE (2006) Dietary overlap and foraging competition between mourning doves and Eurasian collared-doves. J Wildl Manag 70:998–1004CrossRefGoogle Scholar
  33. Pritchard DW (2014) frair: functional response analysis in R. R package version 0.4.
  34. Roy HE, Brown PMJ, Adriaens T, Berkvens N et al (2016) The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol Invasions 18:997–1044CrossRefGoogle Scholar
  35. Sentis A, Hemptinne JL, Brodeur J (2012) Using functional response modelling to investigate the effect of temperature on predator feeding rate and energetic efficiency. Oecologia 169:1117–1125CrossRefGoogle Scholar
  36. Smith CA, Gardiner MM (2013) Biodiversity loss following the introduction of exotic competitors: does intraguild predation explain the decline of native lady beetles? PLoS ONE. Google Scholar
  37. Snell-Rood EC, Swanson EM, Young RL (2015) Life history as a constraint on plasticity: developmental timing is correlated with phenotypic variation in birds. Heredity 115:378–388CrossRefGoogle Scholar
  38. Snyder WE, Clevenger GM, Eigenbrode SD (2004) Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia 140:559–565CrossRefGoogle Scholar
  39. Stemberger RS, Gilbert JJ (1985) Body size, food concentration, and population growth in planktonic rotifers. Ecology 66:1151–1159CrossRefGoogle Scholar
  40. Thiess C, Haenke S, Scherber C, Bengtsson J, Bommarco R, Clement LW, Ceryngier P, Dennis C, Emmerson M, Gagic V, Hawro V, Liira J, Weisser WW, Winqvist C, Tscharntke T (2011) The relationship between agricultural intensification and biological control: experimental tests across Europe. Ecol Appl 21:2187–2196CrossRefGoogle Scholar
  41. Tilman D (1977) Resource competition between plankton algae: an experimental and theoretical approach. Ecology 58:338–348CrossRefGoogle Scholar
  42. Tilman D (1982) Resource competition and community structure. Princeton University Press, New YorkGoogle Scholar
  43. Vilcinskas A, Stoecker K, Schmidtberg H, Röhrich CR, Vogel H (2013) Invasive harlequin ladybird carries biological weapons against native competitors. Science 340:862–863CrossRefGoogle Scholar
  44. Wells ML, McPherson RM (1999) Population dynamics of three coccinellids in flue-cured tobacco and functional response of Hippodamia convergens (Coleoptera; Coccinellidae) feeding on tobacco aphids (Homoptera: Aphididae). Environ Entomol 28:768–773CrossRefGoogle Scholar
  45. Wheeler AG Jr, Hoebeke ER (1995) Coccinella novemnotata in northeastern North America: historical occurrence and current status (Coleoptera: Coccinellidae). Proc Entomol Soc North Wash 97:701–716Google Scholar
  46. Yodzis P, Innes S (1992) Body size and consumer-resource dynamics. Am Nat 139:1151–1175CrossRefGoogle Scholar
  47. Zhao Z-H, Hui C, Ouyang F, Liu J-H, Guan X-Q, He D-H, Ge F (2013) Effects of inter-annual landscape changes on interactions between cereal aphids and their natural enemies. Basic Appl Ecol 14:472–479CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Great Lakes Institute for Environmental ResearchUniversity of WindsorWindsorCanada
  2. 2.Institute for Global Food Security, School of Biological SciencesQueen’s University Belfast, MBCBelfastNorthern Ireland, UK
  3. 3.Biodiversity Institute of OntarioUniversity of GuelphGuelphCanada

Personalised recommendations