Skip to main content
SpringerLink
Log in

Avoidance of intraguild predation leads to a long-term positive trait-mediated indirect effect in an insect community

  • Community ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Intraguild predation among natural enemies is common in food webs with insect herbivores at their base. Though intraguild predation may be reciprocal, typically one species suffers more than the other and frequently exhibits behavioural strategies to lessen these effects. How such short-term behaviours influence population dynamics over several generations has been little studied. We worked with a model insect community consisting of two species of aphid feeding on different host plants (Acyrthosiphon pisum on Vicia and Sitobion avenae on Triticum), a parasitoid (Aphidius ervi) that attacks both species, and a dominant intraguild predator (Coccinella septempunctata) that also feeds on both aphids (whether parasitized or not). As reported previously, we found A. ervi avoided chemical traces of C. septempunctata. In population cages in the laboratory, application of C. septempunctata extracts to Vicia plants reduced parasitism on A. pisum. This did not increase parasitism on the other aphid species, our predicted short-term trait-mediated effect. However, a longer term multigenerational consequence of intraguild predator avoidance was observed. In cages where extracts were applied in the first generation of the study, parasitoid recruitment was reduced leading to higher population densities of both aphid species. S. avenae thus benefits from the presence of a dominant intraguild predator foraging on another species of aphid (A. pisum) on a different food plant, a long-term, trait-mediated example of apparent mutualism. The mechanism underlying this effect is hypothesized to be the reduced searching efficiency of a shared parasitoid in the presence of cues associated with the dominant predator.

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
Fig. 5

Similar content being viewed by others

References

  • Abrams PA (1995) Implications of dynamically variable traits for identifying, classifying, and measuring direct and indirect effects in ecological communities. Am Nat 146:112–134

    Article  Google Scholar 

  • Abrams PA, Menge BA, Mittelbach GG, Spiller D, Yodzis P (1996) Food webs: integration of patterns and dynamics. In: Polis GA, Winemiller KO (eds) Food webs: integration of patterns and dynamics. Chapman and Hall, New York, pp 371–395

    Chapter  Google Scholar 

  • Abrams PA, Holt RD, Roth JD (1998) Apparent competition or apparent mutualism? Shared predation when populations cycle. Ecology 79:201–212

    Article  Google Scholar 

  • Amarasekare P (2008) Coexistence of intraguild predators and prey in resource-rich environments. Ecology 89:2786–2797

    Article  PubMed  Google Scholar 

  • Barribeau SM, Sok D, Gerardo NM (2010) Aphid reproductive investment in response to mortality risks. BMC Evol Biol 10:251

    Article  PubMed Central  PubMed  Google Scholar 

  • Brodeur J, Rosenheim JA (2000) Intraguild interactions in aphid parasitoids. Entomol Exp Appl 97:93–108

    Article  Google Scholar 

  • Brown PMJ, Frost R, Doberski J, Sparks T, Harrington R, Roy HE (2011) Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England. Ecol Entomol 36:231–240

    Article  Google Scholar 

  • Bukovinszky T, Gols R, Hemerik L, Van Lenteren JC, Vet LEM (2007) Time allocation of a parasitoid foraging in heterogeneous vegetation: implications for host-parasitoid interactions. J Anim Ecol 76:845–853

    Article  PubMed  Google Scholar 

  • Choh Y, van der Hammen T, Sabelis MW, Janssen A (2010) Cues of intraguild predators affect the distribution of intraguild prey. Oecologia 163:335–340

    Article  PubMed Central  PubMed  Google Scholar 

  • Cook R (1979) Influential observations in linear regression. J Am Stat Assoc 74:169–174

    Article  Google Scholar 

  • Daza-Bustamante P, Fuentes-Contreras E, Niemeyer HM (2003) Acceptance and suitability of Acyrthosiphon pisum and Sitobion avenae as hosts of the aphid parasitoid Aphidius ervi (Hymenoptera: Braconidae). Eur J Entomol 100:49–53

    Article  Google Scholar 

  • De Vos M, Jander G (2010) Volatile communication in plant-aphid interactions. Curr Opin Plant Biol 13:366–371

    Article  PubMed  Google Scholar 

  • Dicke M (1999) The ecology and evolution of inducible defences. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defences. Princeton, New Jersey, pp 62–88

    Google Scholar 

  • Diehl S, Feissel M (2000) Effects of enrichment on three-level food chains with omnivory. Am Nat 155:200–218

    Article  PubMed  Google Scholar 

  • Dixon AFG, Agarwala BK (1999) Ladybird-induced life-history changes in aphids. Proc R Soc Lond B 266:1549–1553

    Article  Google Scholar 

  • Du YJ, Poppy GM, Powell W, Pickett JA, Wadhams LJ, Woodcock CM (1998) Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. J Chem Ecol 24:1355–1368

    Article  CAS  Google Scholar 

  • Girling RD, Madison R, Hassall M, Poppy GM, Turner JG (2008) Investigations into plant biochemical wound-response pathways involved in the production of aphid-induced plant volatiles. J Exp Bot 59:3077–3085

    Article  CAS  PubMed  Google Scholar 

  • Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, Princeton

    Google Scholar 

  • Gols R, Bukovinszky T, Hemerik L, Harvey JA, Van Lenteren JC, Vet LEM (2005) Reduced foraging efficiency of a parasitoid under habitat complexity: implications for population stability and species coexistence. J Anim Ecol 74:1059–1068

    Article  Google Scholar 

  • Holt RD, Lawton JH (1993) Apparent competition and enemy-free space in insect host-parasitoid communities. Am Nat 142:623–645

    Article  CAS  PubMed  Google Scholar 

  • Holt RD, Lawton JH (1994) The ecological consequences of shared natural enemies. Annu Rev Ecol Syst 25:495–520

    Article  Google Scholar 

  • Holt RD, Polis GA (1997) A theoretical framework for intraguild predation. Am Nat 149:745–764

    Article  Google Scholar 

  • Holt RD, Grover J, Tilman D (1994) Simple rules for interspecific dominance in systems with exploitative and apparent competition. Am Nat 144:741–771

    Article  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 

  • Kunert G, Weisser WW (2003) The interplay between density- and trait-mediated effects in predator-prey interactions: a case study in aphid wing polymorphism. Oecologia 135:304–312

    PubMed  Google Scholar 

  • Letourneau D, Jedlicka J, Bothwell S, Moreno C (2009) Effects of natural enemy biodiversity on the suppression of arthropod herbivores in terrestrial ecosystems. Annu Rev Ecol Evol Syst 40:573–592

    Article  Google Scholar 

  • Lima S (2002) Putting predators back into behavioral predator-prey interactions. Trends Ecol Evol 17:70–75

    Article  Google Scholar 

  • Magalhaes S, Tudorache C, Montserrat M, van Maanen R, Sabelis MW, Janssen A (2005) Diet of intraguild predators affects antipredator behavior in intraguild prey RID B-2657-2009. Behav Ecol 16:364–370

    Article  Google Scholar 

  • Martinou AF, Raymond B, Milonas PG, Wright DJ (2010) Impact of intraguild predation on parasitoid foraging behaviour. Ecol Entomol 35:183–189

    Article  Google Scholar 

  • Meisner M, Harmon JP, Harvey CT, Ives AR (2011) Intraguild predation on the parasitoid Aphidius ervi by the generalist predator Harmonia axyridis: the threat and its avoidance. Entomol Exp Appl 138:193–201

    Article  Google Scholar 

  • Nakashima Y, Senoo N (2003) Avoidance of ladybird trails by an aphid parasitoid Aphidius ervi: active period and effects of prior oviposition experience. Entomol Exp Appl 109:163–166

    Article  Google Scholar 

  • Nakashima Y, Birkett MA, Pye BJ, Pickett JA, Powell W (2004) The role of semiochemicals in the avoidance of the seven-spot ladybird, Coccinella septempunctata, by the aphid parasitoid, Aphidius ervi. J Chem Ecol 30:1103–1116

    Article  CAS  PubMed  Google Scholar 

  • Nakashima Y, Birkett MA, Pye BJ, Powell W (2006) Chemically mediated intraguild predator avoidance by aphid parasitoids: interspecific variability in sensitivity to semiochemical trails of ladybird predators. J Chem Ecol 32:1989–1998

    Article  CAS  PubMed  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York

    Book  Google Scholar 

  • Polis GA, Holt RD (1992) Intraguild predation—the dynamics of complex trophic interactions. Trends Ecol Evol 7:151–154

    Article  CAS  PubMed  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 

  • Raymond B, Darby AC, Douglas AE (2000) Intraguild predators and the spatial distribution of a parasitoid. Oecologia 124:367–372

    Article  Google Scholar 

  • Rosenheim JA, Kaya HK, Ehler LE, Marois JJ, Jaffee BA (1995) Intraguild predation among biological-control agents—theory and evidence. Biol Contr 5:303–335

    Article  Google Scholar 

  • Schmitz O, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163

    Article  Google Scholar 

  • Schmitz OJ, Hawlena D, Trussell GC (2010) Predator control of ecosystem nutrient dynamics. Ecol Lett 13:1199–1209

    Article  PubMed  Google Scholar 

  • Schneider FD, Scheu S, Brose U (2012) Body mass constraints on feeding rates determine the consequences of predator loss. Ecol Lett 15(436):443

    Google Scholar 

  • Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect-plant biology. Oxford University Press, Oxford

    Google Scholar 

  • Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355

    Article  CAS  PubMed  Google Scholar 

  • Straub CS, Snyder WE (2008) Increasing enemy biodiversity strengthens herbivore suppression on two plant species. Ecology 89:1605–1615

    Article  PubMed  Google Scholar 

  • Van Veen FJF, Rajkumar A, Muller C, Godfray HCJ (2001) Increased reproduction by pea aphids in the presence of secondary parasitoids. Ecol Entomol 26:425–429

    Article  Google Scholar 

  • van Veen FJF, Morris RJ, Godfray HCJ (2006) Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annu Rev Entomol 51:187–208

    Article  PubMed  Google Scholar 

  • Van Veen FJF, Mueller C, Pell J, Godfray HCJ (2008) Food web structure of three guilds of natural enemies: predators, parasitoids and pathogens of aphids. J Anim Ecol 77:191–200

    Article  PubMed  Google Scholar 

  • Vance-Chalcraft HD, Soluk DA (2005) Multiple predator effects result in risk reduction for prey across multiple prey densities. Oecologia 144:472–480

    Article  PubMed  Google Scholar 

  • Weisser WW (2000) Metapopulation dynamics in an aphid-parasitoid system. Entomol Exp Appl 97:83–92

    Article  Google Scholar 

  • Weisser WW, Braendle C, Minoretti N (1999) Predator-induced morphological shift in the pea aphid. Proc R Soc Lond B 266:1175–1181

    Article  Google Scholar 

  • Werner E, Peacor S (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100

    Article  Google Scholar 

Download references

Acknowledgments

We especially thank Richard Comont for sharing his expertise in rearing and collecting ladybirds and Clara Torres-Barceló, Piotr Łukasik, Margriet Van Asch, Lee Henry and Ailsa McLean for their help, valuable comments on the experimental set up and discussions. We are also grateful to two anonymous reviewers for their helpful comments. E. F. was funded by the Conselleria d’Educació de la Generalitat Valenciana (Spain) Programa VALi + d per a Investigadors en Fase Postdoctoral programme (APOSTD/2010/062). We also acknowledge support from the E. P. Abraham Cephalosporin Trust.

Author information

Author notes

  1. Enric Frago

    Present address: Laboratory of Entomology, Wageningen University, Droevendaalsesteeg 1, Building 107, Wageningen, The Netherlands

Authors and Affiliations

  1. Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, UK

    Enric Frago & H. Charles J. Godfray

Authors
  1. Enric Frago
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. Charles J. Godfray
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Enric Frago.

Additional information

Communicated by George Heimpel.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 81 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Frago, E., Godfray, H.C.J. Avoidance of intraguild predation leads to a long-term positive trait-mediated indirect effect in an insect community. Oecologia 174, 943–952 (2014). https://doi.org/10.1007/s00442-013-2799-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-013-2799-0

Keywords

Search

Navigation