Skip to main content
Log in

Density-dependent intraguild predation of an aphid parasitoid

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

Abstract

A growing body of research has examined the effect of shared resource density on intraguild predation (IGP) over relatively short time frames. Most of this work has led to the conclusion that when the shared resource density is high, the strength of IGP should be lower, due to prey dilution. However, experiments addressing this topic have been done using micro- or mesocosms that excluded the possibility of intraguild predator aggregation. We examined the effect of shared resource density on IGP of an aphid parasitoid in an open field setting where the effects of prey dilution and predator aggregation could occur simultaneously. We brought potted soybean plants with 2, 20, or 200 soybean aphids (Aphis glycines) and 20 pupae (‘mummies’) of the soybean aphid parasitoid Binodoxys communis into soybean fields in Minnesota, USA. We monitored predator aggregation onto the potted plants, predation of parasitoid mummies, and successful adult emergence of B. communis. We found that predator aggregation was higher at the higher aphid densities on our experimental plants and that this coincided with lower adult emergence of B. communis, indicating that even if a prey dilution effect occurred in our study, it was overcome by short-term predator aggregation. Our results suggest that the effect of shared resource density on IGP may be more nuanced in a field setting than in microcosms due to predator aggregation.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

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

    Article  Google Scholar 

  • Bilu E, Coll M (2007) The importance of intraguild interactions to the combined effect of a parasitoid and a predator on aphid population suppression. Biocontrol 52:753–763

    Article  Google Scholar 

  • Briggs CJ, Borer ET (2005) Why short-term experiments may not allow long-term predictions about intraguild predation. Ecol Appl 15:1111–1117

    Article  Google Scholar 

  • Brodeur J, Rosenheim JA (2000) Intraguild interactions in aphid parasitoids. Entomol Exp Appl 97:98–108

    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 

  • Chacón JM, Landis DA, Heimpel GE (2008) Potential for biotic interference of a classical biological control agent of the soybean aphid. Biol Control 46:216–225

    Article  Google Scholar 

  • Chaneton EJ, Bonsall MB (2000) Enemy-mediated apparent competition: empirical patterns and evidence. Oikos 88:380–394

    Article  Google Scholar 

  • Colfer RG, Rosenheim JA (2001) Predation on immature parasitoids and its impact on aphid suppression. Oecologia 126:292–304

    Article  Google Scholar 

  • Costamagna AC, Landis DA (2006) Predators exert top-down control of soybean aphid across a gradient of agricultural management systems. Ecol Appl 16:1619–1628

    Article  PubMed  Google Scholar 

  • Costamagna AC, Costamagna AC, Landis DA (2007a) Quantifying predation on soybean aphid through direct field observations. Biol Control 42:16–24

    Article  Google Scholar 

  • Costamagna AC, Landis DA, Difonzo CD (2007b) Suppression of soybean aphid by generalist predators results in a trophic cascade in soybeans. Ecol Appl 17:441–451

    Article  PubMed  Google Scholar 

  • Costamagna AC, Landis DA, Brewer MJ (2008) The role of natural enemy guilds in Aphis glycines suppression. Biol Control 45:368–379

    Article  Google Scholar 

  • Daugherty MP, Harmon JP, Briggs CJ (2007) Trophic supplements to intraguild predation. Oikos 116:662–677

    Article  Google Scholar 

  • de Clercq P, Peeters I, Vergauwe 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 SBS, Dordrecht, pp 21–44

    Google Scholar 

  • Desneux N, Barta RJ, Hoelmer KA, Hopper KR, Heimpel GE (2009) Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia 160:387–398

    Article  PubMed  Google Scholar 

  • Donaldson JR, Myers SW, Gratton C (2007) Density-dependent responses of soybean aphid (Aphis glycines Matsumura) populations to generalist predators in mid to late season soybean fields. Biol Control 43:111–118

    Article  Google Scholar 

  • Evans EW (2008) Multitrophic interactions among plants, aphids, alternate prey and shared natural enemies—a review. Eur J Entomol 105:369–380

    Article  Google Scholar 

  • Frank SD, Wratten SD, Sandhu HS, Shrewsbury PM (2007) Video analysis to determine how habitat strata affects predator diversity and predation of Epiphyas postvittana (Lepidoptera : Tortricidae) in a vineyard. Biol Control 41:230–236

    Article  Google Scholar 

  • Heimpel GE, Hough-Goldstein JA (1994) Components of the functional fesponse of Perillus bioculatus (Hemiptera: Pentatomidae). Environ Entomol 23:855–859

    Article  Google Scholar 

  • Heimpel GE, Ragsdale DW, Venette R, Hopper KR, O’Neil RJ, Rutledge CE, Wu Z (2004) Prospects for importation biological control of the soybean aphid: Anticipating potential costs and benefits. Ann Entomol Soc Am 97:249–258

    Article  Google Scholar 

  • Heimpel GE, Frelich LE, Landis DA, Hopper KR, Hoelmer KA, Sezen Z, Asplen MK, Wu K (2010) European buckthorn and Asian soybean aphid as part of an extensive invasional meltdown in North America. Biol Invasions (in press)

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Holt RD (1977) Predation, apparent competition, and structure of prey communities. Theor Popul Biol 12:197–229

    Article  CAS  PubMed  Google Scholar 

  • Holt RD, Huxel GR (2007) Alternative prey and the dynamics of intraguild predation: theoretical perspectives. Ecology 88:2706–2712

    Article  PubMed  Google Scholar 

  • Holt RD, Kotler BP (1987) Short-term apparent competition. Am Nat 130:412–430

    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, vol 3. Springer SBS, Dordrecht, pp 21–44

    Chapter  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Johansson F (1993) Intraguild predation and cannibalism in odonate larvae: effects of foraging behaviour and zooplankton availability. Oikos 66:80–87

    Article  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 

  • 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 

  • Meyhöfer R (2001) Intraguild predation by aphidophagous predators on parasitized aphids: the use of multiple video cameras. Entomol Exp Appl 100:77–87

    Article  Google Scholar 

  • Meyhöfer R, Hindayana D (2000) Effects of intraguild predation on aphid parasitoid survival. Entomol Exp Appl 97:115–122

    Article  Google Scholar 

  • Miao J, Wu K, Hopper KR, Li G (2007) Population dynamics of Aphis Glycines (Homoptera: Aphididae) and impact of natural enemies in northern China. Environ Entomol 36:840–848

    Article  PubMed  Google Scholar 

  • Müller CB, Brodeur J (2002) Intraguild predation in biological control and conservation biology. Biol Control 25:216–223

    Article  Google Scholar 

  • Müller CB, Godfray HCJ (1997) Apparent competition between two aphid species. J Anim Ecol 66:57–64

    Article  Google Scholar 

  • Müller CB, Godfray HCJ (1999) Indirect interactions in aphid-parasitoid communities. Res Popul Ecol 41:93–106

    Article  Google Scholar 

  • Murdoch WW, Chesson J, Chesson PL (1985) Biological control in theory and practice. Am Nat 125:344–366

    Article  Google Scholar 

  • Neuhauser C, Andow DA, Heimpel GE, May G, Shaw RG, Wagenius S (2003) Community genetics: expanding the synthesis of ecology and genetics. Ecology 84:545–558

    Article  Google Scholar 

  • Nóia M, Borges I, Soares AO (2008) Intraguild predation between the aphidophagous ladybird beetles Harmonia axyridis and Coccinella undecimpunctata (Coleoptera: Coccinellidae): the role of intra and extraguild prey densities. Biol Control 46:140–146

    Article  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 

  • Ragsdale DW, Voegtlin DJ, O’Neil RJ (2004) Soybean aphid biology in North America. Ann Entomol Soc Am 97:204–208

    Article  Google Scholar 

  • Ragsdale DW, McCornack BP, Venette RC, Potter BD, Macrae IV, Hodgson EW, O’Neal ME, Johnson KD, O’Neil RJ, DiFonzo CD, Hunt TE, Glogoza PA, Cullen EM (2007) Economic threshold for soybean aphid (Hemiptera: Aphididae). J Econ Entomol 100(4):1258–1267

    Article  CAS  PubMed  Google Scholar 

  • Rickers S, Langel R, Scheu S (2006) Stable isotope analyses document intraguild predation in wolf spiders (Araneae: Lycosidae) and underline beneficial effects of alternative prey and microhabitat structure on intraguild prey survival. Oikos 114:471–478

    Article  Google Scholar 

  • Rosenheim JA, Harmon JP (2006) The influence of intraguild predation on the suppression of a shared prey population: an empirical reassessment. In: Brodeur J, Boivin G (eds) Trophic and guild interactions in biological control. Springer SBS, Dordrecht, pp 1–20

    Chapter  Google Scholar 

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

    Article  Google Scholar 

  • Schellhorn NA, Andow DA (1999a) Cannibalism and interspecific predation: role of oviposition behavior. Ecol Appl 9:418–428

    Google Scholar 

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

    Article  Google Scholar 

  • Schellhorn NA, Andow DA (2005) Response of coccinellids to their aphid prey at different spatial-scales. Pop Ecol 47:71–76

    Article  Google Scholar 

  • Snyder WE, Ives AR (2001) Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82:705–716

    Article  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 

  • Snyder WE, Ballard SN, Yang S, Clevenger GM, Miller TD, Ahn JJ, Hatten TD, Berryman AA (2004) Complementary biocontrol of aphids by the ladybird beetle Harmonia axyridis and the parasitoid Aphelinus asychis on greenhouse roses. Biol Control 30:229–235

    Article  Google Scholar 

  • Vance-Chalcraft HD, Rosenheim JA, Vonesh JR, Osenberg CW, Sih A (2007) The influence of intraguild predation on prey suppression and prey release: a meta-analysis. Ecology 88:2689–2696

    Article  PubMed  Google Scholar 

  • Venette RC, Ragsdale DW (2004) Assessing the invasion by soybean aphid (Homoptera: Aphididae): where will it end? Ann Entomol Soc Am 97:219–226

    Article  Google Scholar 

  • Wyckhuys KAG, Hopper KR, Wu K-M, Straub C, Gratton C, Heimpel GE (2007) Predicting potential ecological impact of soybean aphid biological control introductions. Biocontrol News Info 28:30N–34N

    Google Scholar 

  • Wyckhuys KAG, Stone L, Desneux N, Hoelmer KA, Hopper KR, Heimpel GE (2008) Parasitism of the soybean aphid, Aphis glycines, by Binodoxys communis (Hymenoptera: Braconidae): the role of aphid defensive behavior and parasitoid reproductive performance. Bull Entomol Res 98:361–370

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Jon Malespy, Simon Lueth, Sarah Gunderson, Sheena Ahrar, Mark Asplen, Zeynep Sezen, Christine Dieckhoff, Megan Slaughter, Ashley Chacόn, Daniel Chacόn, and John Chacόn for field and laboratory help. David Andow, Elizabeth Borer, Christine Dieckhoff, and two anonymous reviewers provided helpful suggestions on a previous version of this manuscript. Funding for this work was provided by a United States Environmental Protection Agency (EPA) Science to Achieve Results fellowship to J. Chacón, and also by the University of Minnesota Agricultural Experiment Station. The EPA does not officially endorse this publication and the views expressed herein may not reflect those of the EPA.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeremy Matthew Chacón.

Additional information

Communicated by Sven Bacher.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chacón, J.M., Heimpel, G.E. Density-dependent intraguild predation of an aphid parasitoid. Oecologia 164, 213–220 (2010). https://doi.org/10.1007/s00442-010-1611-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-010-1611-7

Keywords

Navigation