Skip to main content
SpringerLink
Log in

Food web persistence is enhanced by non-trophic interactions

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

Abstract

The strength of interspecific interactions is often proposed to affect food web stability, with weaker interactions increasing the persistence of species, and food webs as a whole. However, the mechanisms that modify interaction strengths, and their effects on food web persistence are not fully understood. Using food webs containing different combinations of predator, prey, and nonprey species, we investigated how predation risk of susceptible prey is affected by the presence of species not directly trophically linked to either predators or prey. We predicted that indirect alterations to the strength of trophic interactions translate to changes in persistence time of extinction-prone species. We assembled interaction webs of protist consumers and turbellarian predators with eight different combinations of prey, predators and nonprey species, and recorded abundances for over 130 prey generations. Persistence of predation-susceptible species was increased by the presence of nonprey. Furthermore, multiple nonprey species acted synergistically to increase prey persistence, such that persistence was greater than would be predicted from the dynamics of simpler food webs. We also found evidence suggesting increased food web complexity may weaken interspecific competition, increasing persistence of poorer competitors. Our results demonstrate that persistence times in complex food webs cannot be predicted from the dynamics of simplified systems, and that species not directly involved in consumptive interactions likely play key roles in maintaining persistence. Global species diversity is currently declining at an unprecedented rate and our findings reveal that concurrent loss of species that modify trophic interactions may have unpredictable consequences for food web stability.

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

Similar content being viewed by others

References

  • Altwegg R, Eng M, Caspersen S, Anholt BR (2006) Functional response and prey defence level in an experimental predator-prey system. Evol Ecol Res 8:115–128

    Google Scholar 

  • Archbold JG, Berger J (1985) A qualitative assessment of some metazoan predators of Halteria grandinella, a common freshwater ciliate. Hydrobiologia 126:97–102

    Article  Google Scholar 

  • Bonsall MB, French DR, Hassell MP (2002) Metapopulation structures affect persistence of predator-prey interactions. J Anim Ecol 71:1075–1084

    Article  Google Scholar 

  • Borrvall C, Ebenman B (2006) Early onset of secondary extinctions in ecological communities following the loss of top predators. Ecol Lett 9:435–442

    Article  PubMed  Google Scholar 

  • Cardinale BJ et al (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67

    Article  CAS  PubMed  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • Crowder LB, Cooper WE (1982) Habitat structural complexity and the interaction between bluegills and their prey. Ecology 63:1802–1813

    Article  Google Scholar 

  • Duffy JE (2009) Why biodiversity is important to the functioning of real-world ecosystems. Front Ecol Environ 7:437–444

    Article  Google Scholar 

  • Dunne JA, Williams RJ (2009) Cascading extinctions and community collapse in model food webs. Philos Trans R Soc Lond B 364:1711–1723

    Article  Google Scholar 

  • Edwards KF, Aquilino KM, Best RJ, Sellheim KL, Stachowicz JJ (2010) Prey diversity is associated with weaker consumer effects in a meta-analysis of benthic marine experiments. Ecol Lett 13:194–201

    Article  PubMed  Google Scholar 

  • Fenchel T (1980) Suspension feeding in ciliated protozoa: functional response and particle size selection. Microb Ecol 6:1–11

    Article  CAS  PubMed  Google Scholar 

  • Golubski AJ, Abrams PA (2011) Modifying modifiers: what happens when interspecific interactions interact? J Anim Ecol 80:1097–1108

    Article  PubMed  Google Scholar 

  • Hammill E, Kratina P, Anholt BR (2009) Non-lethal presence of predators modifies morphology and movement rates in Euplotes. Hydrobiologia 621:183–189

    Article  Google Scholar 

  • Hammill E, Petchey OL, Anholt BR (2010) Predator functional response changed by induced defenses in prey. Am Nat 176:723–731

    Article  PubMed  Google Scholar 

  • Harrell FJ (2001) Regression modelling strategies. Springer, New York

    Book  Google Scholar 

  • Hillebrand H, Cardinale BJ (2004) Consumer effects decline with prey diversity. Ecol Lett 7:192–201

    Article  Google Scholar 

  • Holling CS (1959) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–389

    Article  Google Scholar 

  • Holyoak M, Lawler SP, Robert AD (2005) The contribution of laboratory experiments on protists to understanding population and metapopulation dynamics. Adv Ecol Res 37:245–271

    Article  Google Scholar 

  • Hutchinson G (1961) Paradox of plankton. Am Nat 95:137–145

    Article  Google Scholar 

  • Ihalainen E, Rowland HM, Speed MP, Ruxton GD, Mappes J (2012) Prey community structure affects how predators select for Mullerian mimicry. Proc R Soc Lond B 279:2099–2105

    Article  Google Scholar 

  • Jeschke JM, Kopp M, Tollrian R (2002) Predator functional responses: discriminating between handling and digesting prey. Ecol Monogr 72:95–112

    Article  Google Scholar 

  • Kratina P, Vos M, Anholt BR (2007) Species diversity modulates predation. Ecology 88:1917–1923

    Article  PubMed  Google Scholar 

  • Kratina P, Vos M, Bateman A, Anholt BR (2009) Functional responses modified by predator density. Oecologia 159:425–433

    Article  PubMed  Google Scholar 

  • Kratina P, Hammill E, Anholt BR (2010) Stronger inducible defences enhance persistence of intraguid prey. J Anim Ecol 79:993–999

    Article  PubMed  Google Scholar 

  • Kusch J, Kuhlmann HW (1994) Cost of Stenostomum induced morphological defense in the ciliate Euplotes octocarinatus. Arch Hydrobiol 130:257–267

    Google Scholar 

  • Lawler SP, Morin PJ (1993) Food web architecture and population dynamics in laboratory microcosms of protists. Am Nat 141:675–686

    Article  CAS  PubMed  Google Scholar 

  • Loreau M, de Mazancourt C (2013) Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol Lett 16:106–115

    Article  PubMed  Google Scholar 

  • Lyons KG, Schwartz MW (2001) Rare species loss alters ecosystem function—invasion resistance. Ecol Lett 4:358–365

    Article  Google Scholar 

  • McCann KS (2000) The diversity-stability debate. Nature 405:228–233

    Article  CAS  PubMed  Google Scholar 

  • McCann K, Hastings A, Huxel GR (1998) Weak trophic interactions and the balance of nature. Nature 395:794–798

    Article  CAS  Google Scholar 

  • Morin PJ (1986) Interactions between intraspecific competition and predation in an amphibian predator-prey system. Ecology 67:713–720

    Article  Google Scholar 

  • Nandini S, Sarma SSS, Dumont H (2011) Predatory and toxic effects of the turbellarian (Stenostomum cf leucops) on the population dynamics of Euchlanis dilatata, Plationus patulus (Rotifera) and Moina macrocopa (Cladocera). Hydrobiologia 662:171–177

    Article  CAS  Google Scholar 

  • Nuttycombe JW, Waters AJ (1935) Feeding habits and pharyngeal structure in Stenostomum. Biol Bull 69:439–446

    Article  Google Scholar 

  • Petchey OL et al (2004) Species loss and the structure and functioning of multitrophic aquatic systems. Oikos 104:467–478

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Ricci C (1984) Culturing of some bdelloid rotifers. Hydrobiologia 112:45–51

    Article  Google Scholar 

  • Srivastava DS (2006) Habitat structure, trophic structure and ecosystem function: interactive effects in a bromeliad-insect community. Oecologia 149:493–504

    Article  PubMed  Google Scholar 

  • Staddon P, Lindo Z, Crittenden PD, Gilbert F, Gonzalez A (2010) Connectivity, non-random extinction and ecosystem function in experimental metacommunities. Ecol Lett 13:543–552

    Article  PubMed  Google Scholar 

  • Thompson R, Starzomski BM (2007) What does biodiversity actually do? A review for managers and policy makers. Biodivers Cons 16:1359–1378

    Article  Google Scholar 

  • van der Stap I, Vos M, Tollrian R, Mooij WM (2008) Inducible defenses, competition and shared predation in planktonic food chains. Oecologia 157:697–705

    Article  PubMed  Google Scholar 

  • Vos M, Berrocal SM, Karamaouna F, Hemerik L, Vet LEM (2001) Plant-mediated indirect effects and the persistence of parasitoid-herbivore communities. Ecol Lett 4:38–45

    Article  Google Scholar 

  • Wootton JT (1992) Indirect effects, prey susceptibility, and habitat selection—impacts of birds on limpets and algae. Ecology 73:981–991

    Article  Google Scholar 

  • Worsfold NT, Warren PH, Petchey OL (2009) Context-dependent effects of predator removal from experimental microcosm communities. Oikos 118:1319–1326

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank Anita Narwani, Trisha Atwood and Finn Hamilton for their insightful comments and discussions. Earlier versions of this work were substantially improved by the efforts of Scott Peacor and two anonymous reviewers. Stephanie Lingard provided invaluable laboratory support. This work was funded by the Canada Research Chairs program and a NSERC Discovery Grant awarded to B.R.A.

Conflict of interest

The authors have no conflicts of interest to declare. All applicable institutional and/or national guidelines for the care and use of animals were followed.

Author information

Authors and Affiliations

  1. School of the Environment, University of Technology Sydney, Sydney, Australia

    Edd Hammill

  2. School of Biological and Chemical Sciences, Queen Mary University of London, London, UK

    Pavel Kratina

  3. Department of Zoological Biodiversity, Ruhr-Universität Bochum, Universitätsstr. 150/Gebäude ND05, 44780, Bochum, Germany

    Matthijs Vos

  4. Department of Aquatic Ecology, Netherlands Institute of Ecology, Royal Netherlands Academy of Arts and Sciences (NIOO-KNAW), Wageningen, The Netherlands

    Matthijs Vos

  5. Institute for Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland

    Owen L. Petchey

  6. Bamfield Marine Science Centre, 100 Pachena Road, Bamfield, BC, Canada

    Bradley R. Anholt

  7. Department of Biology, University of Victoria, Victoria, BC, Canada

    Bradley R. Anholt

Authors
  1. Edd Hammill
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pavel Kratina
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthijs Vos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Owen L. Petchey
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bradley R. Anholt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Edd Hammill.

Additional information

Communicated by Scott D. Peacor.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 198 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hammill, E., Kratina, P., Vos, M. et al. Food web persistence is enhanced by non-trophic interactions. Oecologia 178, 549–556 (2015). https://doi.org/10.1007/s00442-015-3244-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3244-3

Keywords

Search

Navigation