Skip to main content
Log in

Emergent impacts of cannibalism and size refuges in prey on intraguild predation systems

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

Abstract

Many organisms undergo ontogenetic niche shifts due to considerable changes in size during their development. These ontogenetic shifts can alter the trophic position of individuals, the type and strength of ecological interactions across species, and allow for cannibalism within species. In this study we ask if and how the interaction of a size refuge and cannibalism in the prey alters the dynamics of intraguild predation (IGP) systems. By manipulating the composition of large cannibalistic (Aeshna umbrosa) and predatory (Anax junius) dragonfly larvae in mesocosms we show that the interaction of cannibals and predators was non-linear and increased the survival of prey. The structure of the final resource community shared by prey and predator differed between small and large dragonfly treatments but not within size classes across species. In general, the small prey stage showed similar shifts in microhabitat use and refuge use when exposed to either conspecific cannibals or predators, while large cannibals showed no clear anti-predator response. However, further behavioral experiments revealed that specific behavioral components, such as distances between individuals or number of movements, differed when individuals were exposed to either cannibals or predators. This indicates that individuals discriminated between conspecific or heterospecific predators. Furthermore, in similar experiments large cannibals and predators showed different behaviors when exposed to conspecifics rather than to each other. These changes in behavior are consistent with the observed increase in prey survival. In general, the results indicate that cannibalism and ontogenetic niche shifts can result in behavior-mediated indirect interactions that reduce the impact of the predator on the mortality of its prey and alter the interactions of IGP systems. However, they also indicate that size is not the sole determinant and that we also need to account for the species identity when predicting the dynamics of communities.

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
Fig. 5

Similar content being viewed by others

References

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Article  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289

    Google Scholar 

  • Biro PA, Post JR, Parkinson EA (2003) From individuals to populations: prey fish risk-taking mediates mortality in whole-system experiments. Ecology 84:2419–2431

    Article  Google Scholar 

  • Briggs CJ (1993) Competition among parasitoid species on a stage-structured host and its effect on host suppression. Am Nat 141:372–397

    Article  Google Scholar 

  • Burgio G, Santi F, Miani S (2005) Intra-guild predation and cannibalism between Harmonia axyridis and Adalia bipunctata adults and larvae: laboratory experiments. Bull Insectol 58:135–140

    Google Scholar 

  • Bystrom P, Persson L, Wahlstrom E (1998) Competing predators and prey: juvenile bottlenecks in whole-lake experiments. Ecology 79:2153–2167

    Google Scholar 

  • Bystrom P, Persson L, Wahlstrom E, Westman E (2003) Size- and density-dependent habitat use in predators: consequences for habitat shifts in young fish. J Anim Ecol 72:156–168

    Article  Google Scholar 

  • Cameron TC, Wearing HJ, Rohr JR, Sait SM (2007) Two-species asymmetric competition: effects of age structure on intra- and interspecifci interactions. J Anim Ecol 76:83–93

    Article  PubMed  Google Scholar 

  • Claus-Walker DB, Crowley PH, Johansson F (1997) Fish predation, cannibalism, and larval development in the dragonfly Epitheca cynosura. Can J Zool 75:687–696

    Article  Google Scholar 

  • Corbet PS (1999) Dragonflies: behavior and ecology of Odonata. Cornell University Press, Ithaca

    Google Scholar 

  • Crowley PH, Dillon PM, Johnson DM, Watson CN (1987) Intraspecific interference among larvae in a semivoltine dragonfly population. Oecologia 71:447–456

    Article  Google Scholar 

  • Crumrine P (2005) Size structure and substitutability in an odonate intraguild predation system. Oecologia 145:132–139

    Article  PubMed  Google Scholar 

  • Crumrine PW, Crowley PH (2003) Partitioning components of risk reduction in a dragonfly-fish intraguild predation system. Ecology 84:1588–1597

    Article  Google Scholar 

  • Fox LR (1975) Cannibalism in natural populations. Annu Rev Ecol Syst 6:87–106

    Article  Google Scholar 

  • Gerber GP, Echternacht AC (2000) Evidence for asymmetrical intraguild predation between native and introduced Anolis lizards. Oecologia 124:599

    Article  Google Scholar 

  • Greenberg LA, Bergman E, Eklov AG (1997) Effects of predation and intraspecific interactions on habitat use and foraging by brown trout in artificial streams. Ecol Freshwater Fish 6:16–26

    Article  Google Scholar 

  • Griffen B (2006) Detecting emergent effects of multiple predator species. Oecologia 148:702

    Article  PubMed  Google Scholar 

  • Griffen B, Byers J (2006a) Partitioning mechanisms of predator interference in different habitats. Oecologia 146:608–614

    Article  PubMed  Google Scholar 

  • Griffen BD, Byers JE (2006b) Intraguild predation reduces redundancy of predator species in multiple predator assemblage. J Anim Ecol 75:959–966

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Hopper KR, Crowley PH, Kielman D (1996) Density dependence, hatching synchrony, and within-cohort cannibalism in young dragonfly larvae. Ecology 77:191–200

    Article  Google Scholar 

  • Keren-Rotem T, Bouskila A, Geffen E (2006) Ontogenetic habitat shift and risk of cannibalism in the common chameleon (Chamaeleo chamaeleon). Behav Ecol Sociobiol 59:723

    Article  Google Scholar 

  • Lima SL (1998) Nonlethal effects in the ecology of predator–prey interactions—what are the ecological effects of anti-predator decision-making? Bioscience 48:25–34

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, Cary

    Google Scholar 

  • Magalhaes S, Janssen A, Montserrat M, Sabelis MW (2005) Prey attack and predators defend: counterattacking prey trigger parental care in predators. Proc R Soc B Biol Sci 272:1929–1933

    Article  Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  • McPeek MA (1990) Determination of species composition in the Enallagma damselfly assemblages of permanent lakes. Ecology 71:83–98

    Article  Google Scholar 

  • Mylius SD, Klumpers K, de Roos AM, Persson L (2001) Impact of intraguild predation and stage structure on simple communities along a productivity gradient. Am Nat 158:259–276

    Article  PubMed  CAS  Google Scholar 

  • Olson MH, Mittelbach GG, Osenberg CW (1995) Competition between predator and prey—resource-based mechanisms and implications for stage-structured dynamics. Ecology 76:1758–1771

    Article  Google Scholar 

  • Osenberg CW, Mittelbach GG, Wainwright PC (1992) 2-stage life histories in fish: the interaction between juvenile competition and adult performance. Ecology 73:255–267

    Article  Google Scholar 

  • Persson L (1988) Asymmetries in competitive and predatory interactions in fish populations. In: Ebenman B, Persson L (eds) Size-structured populations—ecology and evolution. Springer, Berlin, pp 203–218

    Google Scholar 

  • Persson L (1999) Trophic cascades: abiding heterogeneity and the trophic level concept at the end of the road. Oikos 85:385–397

    Article  Google Scholar 

  • Persson L, Eklov P (1995) Prey refuges affecting interactions between piscivorous perch and juvenile perch and roach. Ecology 76:70–81

    Article  Google Scholar 

  • Persson L, Greenberg LA (1990) Juvenile competitive bottlenecks: the perch (Perca fluviatilis)–Roach (Rutilus rutilus) interaction. Ecology 71:44

    Article  Google Scholar 

  • Persson L et al (2003) Gigantic cannibals driving a whole-lake trophic cascade. Proc Natl Acad Sci USA 100:4035–4039

    Article  PubMed  CAS  Google Scholar 

  • Polis GA (1984) Age structure component of niche width and intraspecific resource partitioning: can age groups function as ecological species? Am Nat 123:541–564

    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 

  • Rettig JE, Mittelbach GG (2002) Interactions between adult and larval bluegill sunfish: positive and negative effects. Oecologia 130:222–230

    Google Scholar 

  • Rudolf VHW (2006) The influence of size-specific indirect interactions in predator-prey systems. Ecology 87:362–371

    Article  PubMed  Google Scholar 

  • Rudolf VHW (2007a) Consequences of stage-structured predators: cannibalism, behavioral effects and trophic cascades. Ecology 88:2991–3003

    Article  PubMed  Google Scholar 

  • Rudolf VHW (2007b) The interaction of cannibalism and omnivory: consequences for community dynamics. Ecology 88:2697–2705

    Article  PubMed  Google Scholar 

  • Rudolf VHW (2008a) The impact of cannibalism in the prey on predator-prey systems. Ecology (in press)

  • Rudolf VHW (2008b) Impact of cannibalism on predator–prey dynamics: size-structured interactions and apparent mutualism. Ecology 89:1650–1660

    Google Scholar 

  • Schmitz OJ (2007) Predator diversity and trophic interactions. Ecology 88:2415–2426

    Article  PubMed  Google Scholar 

  • Sih A (1982) Foraging strategies and the avoidance of predation by an aquatic insect, Notonecta hoffmanni. Ecology 63:786–796

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Soluk DA, Collins NC (1988) Synergistic interactions between fish and stoneflies—facilitation and interference among stream predators. Oikos 52:94–100

    Article  Google Scholar 

  • Taylor RC, Trexler JC, Loftus WF (2001) Separating the effects of intra- and interspecific age-structured interactions in an experimental fish assemblage. Oecologia 127:143–152

    Article  Google Scholar 

  • Tolonen KT, Hämäläinen H, Holopainen IJ, Mikkonen K, Karjalainen J (2003) Body size and substrate association of littoral insects in relation to vegetation structure. Hydrobiologia 499:179–190

    Article  Google Scholar 

  • Van Buskirk J (1989) Density-dependent cannibalism in larval dragonflies. Ecology 70:1442–1449

    Article  Google Scholar 

  • Van Buskirk J (1992) Competition, cannibalism, and size class dominance in a dragonfly. Oikos 65:455–464

    Article  Google Scholar 

  • Van Buskirk J (1993) Population consequences of larval crowding in the dragonfly Aeshna juncea. Ecology 74:1950–1958

    Article  Google Scholar 

  • van de Wolfshaar KE, de Roos AM, Persson L (2006) Size-dependent interactions inhibit coexistence in intraguild predation systems with life-history omnivory. Am Nat 168:62–75

    Article  PubMed  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(11):2689–2696

    Article  PubMed  Google Scholar 

  • Wahlstrom E, Persson L, Diehl S, Bystrom P (2000) Size-dependent foraging efficiency, cannibalism and zooplankton community structure. Oecologia 123:138–148

    Article  Google Scholar 

  • Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size structured populations. Annu Rev Ecol Syst 15:393–425

    Article  Google Scholar 

  • Werner EE, Hall DJ (1988) Ontogenetic habitat shifts in bluegill: the foraging rate-predation risk trade-off. Ecology 69:1352–1366

    Article  Google Scholar 

  • Wissinger SA (1988) Effects of food availability on larval development and inter-instar predation among larvae of Libellula lydia and Libellula luctuosa (Odonata, Anisoptera). Can J Zool 66:543–549

    Article  Google Scholar 

  • Wissinger SA (1992) Niche overlap and the potential for competition and intraguild predation between size-structured populations. Ecology 73:1431–1444

    Article  Google Scholar 

  • Wissinger S, McGrady J (1993) Intraguild predation and competition between larval dragonflies—direct and indirect effects on shared prey. Ecology 74:207–218

    Article  Google Scholar 

  • Woodward G, Hildrew AG (2002) Body-size determinants of niche overlap and intraguild predation within a complex food web. J Anim Ecol 71:1063–1074

    Article  Google Scholar 

  • Woodward G, Speirs DC, Hildrew AG, Hal C (2005) Quantification and resolution of a complex, size-structured food web. Adv Ecol Res 36:85–135

    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

    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

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank H. Wilbur and P. Crumrine for helpful comments on experimental design and set up, and A. Dunham for valuable comments on previous versions of the manuscript. This research was supported by the NSF grant DBI-0453380 and DEB 0608346. All experiments comply with the current laws of the United States.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Volker H. W. Rudolf.

Additional information

Communicated by Geoffrey Trussell.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1 (DOC 98 kb)

Table S2 (DOC 98 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rudolf, V.H.W., Armstrong, J. Emergent impacts of cannibalism and size refuges in prey on intraguild predation systems. Oecologia 157, 675–686 (2008). https://doi.org/10.1007/s00442-008-1107-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-008-1107-x

Keywords

Navigation