Skip to main content
Log in

Effect of size, extraguild prey and habitat complexity on intraguild interactions: a case study with the invasive ladybird Harmonia axyridis and the hoverfly Episyrphus balteatus

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

Intraguild predation (IGP) is a widespread interaction between predatory arthropods, and is influenced by several factors. The harlequin ladybird, Harmonia axyridis (Coleoptera: Coccinellidae), has frequently been reported as an intraguild predator of other Coccinellidae, but little is known about its interactions with other aphidophagous predators, including syrphids. This study investigated the incidence of IGP between H. axyridis and Episyrphus balteatus (Diptera: Syrphidae), the most abundant hoverfly species in Europe and a commercially available aphid biocontrol agent. The influence of size, presence of extraguild prey and habitat complexity were investigated through laboratory experiments in Petri dishes and on potted broad bean plants. In both types of arenas, IGP between H. axyridis and E. balteatus was found to be asymmetric, with the coccinellid in the majority of cases being the intraguild predator. There was a significant effect of size on the frequency of IGP. The efficiency of H. axyridis as an intraguild predator increased with the developmental stage. Early instars of E. balteatus were the most vulnerable to IGP. Pupae of either species were not attacked. In the presence of extraguild prey, the frequency of IGP was substantially reduced. However, IGP still occurred, mainly in combinations of older larvae of H. axyridis with first or second instars of E. balteatus. The size of the arena affected the incidence of IGP in combinations with second instars of E. balteatus, but not in combinations with third instars. Field research is needed to elucidate the ecological relevance of IGP among these predators.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

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 

  • Alhmedi A, Haubruge E, Bodson B, Francis F (2007) Aphidophagous guilds on nettle (Urtica dioica) strips close to fields of green pea, rape and wheat. Insect Sci 14:419–424

    Article  Google Scholar 

  • Alhmedi A, Haubruge E, Francis F (2010) Intraguild interactions and aphid predators: biological efficiency of Harmonia axyridis and Episyrphus balteatus. J Appl Entomol 134:34–44

    Article  Google Scholar 

  • Almohamad R, Verheggen FJ, Francis F, Haubruge E (2010) Intraguild interactions between the predatory hoverfly Episyrphus balteatus (Diptera: Syrphidae) and the Asian ladybird, Harmonia axyridis (Coleoptera: Coccinellidae): effect of larval tracks. Eur J Entomol 107:41–45

    Google Scholar 

  • Altman M, Gill J, McDonald MP (2004) Numerical issues in statistical computing for the social scientist. Wiley, Hoboken

    Google Scholar 

  • 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 

  • Arim M, Marquet PA (2004) Intraguild predation: a widespread interaction related to species biology. Ecol Lett 7:557–564

    Article  Google Scholar 

  • Berkvens N, Bonte J, Berkvens D, Deforce K, Tirry L, De Clercq P (2008) Pollen as an alternative food for Harmonia axyridis. BioControl 53:201–210

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Burgio G, Santi F, Maini S (2002) On intra-guild predation and cannibalism in Harmonia axyridis (Pallas) and Adalia bipunctata L. (Coleoptera: Coccinellidae). Biol Control 24:110–116

    Article  Google Scholar 

  • Chang GC (1996) Comparison of single versus multiple species of generalist predators for biological control. Environ Entomol 25:207–212

    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 (2005) Predation and cannibalism of lady beetle eggs by adult lady beetles. Biol Control 34:159–164

    Article  Google Scholar 

  • Cottrell TE, Yeargan KV (1998) Intraguild predation between an introduced lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae), and a native lady beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). J Kans Entomol Soc 71:159–163

    Google Scholar 

  • Coutanceau JP (2006) Harmonia axyridis (Pallas, 1773) : une coccinelle asiatique introduite, acclimatée et en extension en France. Bull Soc Entomol France 111:395–401

    Google Scholar 

  • Day WH, Prokrym DR, Ellis DR, Chianese RJ (1994) The known distribution of the predator Propylea quattuordecimpunctata (Coleoptera, Coccinellidae) in the United States, and thoughts on the origin of this species and 5 other exotic lady beetles in eastern North-America. Entomol News 105:244–256

    Google Scholar 

  • De Clercq P, Peeters I, Vergrauwe G, 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 

  • Denno RF, Finke DL (2006) Multiple predator interactions and food-web connectance: implications for biological control. In: Brodeur J, Boivin G (eds) Trophic and guild interactions in biological control. Springer, Dordrecht, pp 45–70

    Chapter  Google Scholar 

  • 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 

  • Frechette B, Rojo S, Alomar O, Lucas E (2007) Intraguild predation between syrphids and mirids: who is the prey? Who is the predator? BioControl 52:175–191

    Article  Google Scholar 

  • Gardiner MM, Landis DA (2007) Impact of intraguild predation by adult Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Hemiptera: Aphididae) biological control in cage studies. Biol Control 40:386–395

    Article  Google Scholar 

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

    Google Scholar 

  • Hindayana D, Meyhofer R, Scholz D, Poehling HM (2001) Intraguild predation among the hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and other aphidophagous predators. Biol Control 20:236–246

    Article  Google Scholar 

  • Hodek I, Honek A (1996) Ecology of Coccinellidae. Kluwer, Dordrecht

    Google Scholar 

  • Hoogendoorn M, Heimpel GE (2004) Competitive interactions between an exotic and a native ladybeetle: a field cage study. Entomol Exp Appl 111:19–28

    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. Springer, Dordrecht, pp 21–40

    Chapter  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kajita Y, Takano F, Yasuda H, Agarwala BK (2000) Effects of indigenous ladybird species (Coleoptera: Coccinellidae) on the survival of an exotic species in relation to prey abundance. Appl Entomol Zool 35:473–479

    Article  Google Scholar 

  • Kajita Y, Takano F, Yasuda H, Evans EW (2006) Interactions between introduced and native predatory ladybirds (Coleoptera, Coccinellidae): factors influencing the success of species introductions. Ecol Entomol 31:58–67

    Article  Google Scholar 

  • 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 

  • Koch RL, Venette RC, Hutchison WD (2006) Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the Western Hemisphere: implications for South America. Neotrop Entomol 35:421–434

    Article  PubMed  Google Scholar 

  • Levin SA (1992) The problem of pattern and scale in ecology. Ecology 73:1943–1967

    Article  Google Scholar 

  • Lombaert E, Guillemaud T, Cornuet JM, Malausa T, Facon B, Estoup A (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. Plos One 5: Artn E9743. doi:10.1371/Journal.Pone.0009743

  • Lucas E (2005) Intraguild predation among aphidophagous predators. Eur J Entomol 102:351–363

    Google Scholar 

  • Lucas E, Coderre D, Brodeur J (1998) Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79:1084–1092

    Article  Google Scholar 

  • Majerus M, Strawson V, Roy H (2006) The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecol Entomol 31:207–215

    Article  Google Scholar 

  • McCornack BP, Koch RL, Ragsdale DW (2007) A simple method for in-field sex determination of the multicolored Asian lady beetle Harmonia axyridis. J Insect Sci 7:1–12

    Article  PubMed  CAS  Google Scholar 

  • McCullagh P, Nelder J (1989) Generalized linear models. Chapman and Hall, London

    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, 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 

  • Obrycki JJ, Giles KL, Ormord AM (1998) Interactions between an introduced and indigenous coccinellid species at different prey densities. Oecologia 117:279–285

    Article  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 

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

    Article  Google Scholar 

  • Phoofolo MW, Obrycki JJ (1998) Potential for intraguild predation and competition among predatory Coccinellidae and Chrysopidae. Entomol Exp Appl 89:47–55

    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 

  • Putra NS, Yasuda H, Sato S (2009) Oviposition preference of two hoverfly species in response to risk of intraguild predation. Appl Entomol Zool 44:29–36

    Article  Google Scholar 

  • Sadeghi H, Gilbert F (2000) Aphid suitability and its relationship to oviposition preference in predatory hoverflies. J Anim Ecol 69:771–784

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Sato S, Dixon AFG, Yasuda H (2003) Effect of emigration on cannibalism and intraguild predation in aphidophagous ladybirds. Ecol Entomol 28:628–633

    Article  Google Scholar 

  • Sengonca C, Frings B (1985) Interference and competitive behavior of the aphid predators, Chrysoperla carnea and Coccinella septempunctata in the laboratory. Entomophaga 30:245–251

    Article  Google Scholar 

  • Shellhorn NA, Andow DA (1999) Mortality of coccinellid (Coleoptera: Coccinellidae) larvae and pupae when prey become scarce. Environ Entomol 28:1092–1100

    Google Scholar 

  • Snyder WE, Ives AR (2003) Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology 84:91–107

    Article  Google Scholar 

  • SPSS Inc. (2006) SPSS base user’s guide. SPSS Inc., Chicago

  • Stubbs AE, Falk SJ (2002) British hoverflies: an illustrated identification guide. British Entomological and Natural History Society, Reading

    Google Scholar 

  • Tenhumberg B (1995) Estimating predatory efficiency of Episyrphus balteatus (Diptera, Syrphidae) in cereal fields. Environ Entomol 24:687–691

    Google Scholar 

  • Tenhumberg B, Poehling HM (1995) Syrphids as natural enemies of cereal aphids in Germany: aspects of their biology and efficacy in different years and regions. Agric Ecosyst Environ 52:39–43

    Article  Google Scholar 

  • Verlinden L, Decleer K (1987) The hoverflies (Diptera, Syrphidae) of Belgium and their faunistics: frequency, distribution, phenology. Koninklijk Belgisch Instituut voor Natuurwetenschappen, Brussel

    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

    Article  Google Scholar 

  • Yasuda H, Kikuchi T, Kindlmann P, Sato S (2001) Relationships between attack and escape rates, cannibalism, and intraguild predation in larvae of two predatory ladybirds. J Insect Behav 14:373–384

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by a grant from the Research Foundation—Flanders (FWO Vlaanderen) to Brecht Ingels. We are grateful to Nick Berkvens and Dirk Berkvens for their help with the statistical analyses. We also thank two anonymous reviewers and the associate editor for their helpful comments and suggestions, which greatly improved this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brecht Ingels.

Additional information

Handling Editor: Arne Janssen

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ingels, B., De Clercq, P. Effect of size, extraguild prey and habitat complexity on intraguild interactions: a case study with the invasive ladybird Harmonia axyridis and the hoverfly Episyrphus balteatus . BioControl 56, 871–882 (2011). https://doi.org/10.1007/s10526-011-9363-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-011-9363-9

Keywords

Navigation