Nonconsumptive Effects of Predators and Trait‐Mediated Indirect Effects

Scott D Peacor, Michigan State University, East Lansing, Michigan, USA
Earl E Werner, University of Michigan, Ann Arbor, Michigan, USA

Published online: December 2008

DOI: 10.1002/9780470015902.a0021216

Phenotypic plasticity in species’ traits is ubiquitous across taxa and habitats. This plasticity can affect the qualitative and quantitative nature of species interactions and thereby affect food webs. Empirical work has focused on predator–prey interactions, in part because most prey respond to predator presence through a suite of traits that reduce risk. These responses can incur costs in fitness correlates (e.g. growth and survival) of the prey, i.e. are nonconsumptive effects (NCEs) of predators. Further, these responses can lead to indirect effects transmitted through the prey to other species in the food web, termed trait-mediated indirect effects (TMIEs). NCEs and TMIEs have been demonstrated in a wide range of communities and across diverse taxa. These effects can contribute substantially to the influence of predators (including through competition, trophic cascades and keystone predation), and therefore can play a critical role in the dynamics and structure of ecological communities.

Key concepts

  • Phenotypic plasticity in species traits is widespread and represented across diverse taxa and ecosystems.
  • To reduce predation risk, organisms respond to predator (including herbivore) presence by modifying traits, including developmental, morphological, physiological, life historical and behavioural characteristics.
  • Phenotypic responses to predators often incur a cost to prey fitness correlates such as growth rate and survival. These costs to fitness are termed nonconsumptive effects (NCEs) of the predator on its prey, to distinguish them from the consumptive effects (CEs) due to predation.
  • Phenotypic responses by prey to predators alter the nature of the interactions between prey and other (third) species. The predator is said to have a trait-mediated indirect effect (TMIE) on the third species through induced changes in the intermediate species’ (prey's) traits.
  • Predator-induced changes in prey traits can lead to TMIEs of the predator on prey resources (resulting in trait-mediated trophic cascades), prey competitors and other predators of the prey.
  • NCEs and TMIEs can qualitatively change the nature of species interactions. For example, predator-induced changes in prey traits can reverse competitive interactions, and lead to increases in prey growth rates due to strong TMIEs on prey resources.
  • NCEs and TMIEs can contribute strongly, and even dominate, the net effect of predators on prey and net indirect effect of the predator on species the prey interacts with. Thus, they can strongly affect prey population growth rates, community structure and ecosystem processes.
  • Factors, such as temperature, resource growth rates, prey density and prey–competitor density, can strongly influence the magnitude of NCEs and TMIEs.
  • It will be necessary to formally incorporate phenotypic responses of prey to predators into the conceptual foundations of ecology and strategies for the management of ecological systems.

Keywords: nonconsumptive; trait-mediated; food web; phenotypic plasticity; indirect interaction

Figure 1. The diagram illustrates the difference between fixed and plastic phenotypic responses to predator risk. Zooplanktons are distributed high in the water column at night (panel a), but migrate to deeper (and darker) water levels to avoid predation risk during the day (panels b and c). Panel (b) illustrates a fixed response to a proximate signal such as light level, i.e. zooplanktons are lower in the water column independent of fish density. Panel (c) illustrates a plastic response, i.e. vertical migration increases as a function of fish density. NCEs will result from the plastic response, but not from the fixed response.
Figure 2. Diagrams of NCEs and TMIEs. Strait arrows represent consumptive effects. Curved arrows represent a predator-induced change in prey phenotype. Each figure illustrates a species in a different position (represented by shading of the letter) in a simple food web (or chain) affected by the predator. The figure illustrates NCEs and TMIEs with increasing complexity. First, a predator-induced change in prey phenotype can affect fitness correlates of the prey (a). These changes in prey traits can also affect the interaction of the prey with other species, causing a TMIE of the predator on these other species, e.g. prey resources (b) or other predators of the prey (c). TMIEs with more links are also illustrated, e.g. with three links in which the predator affects a competitor (i.e. consumes the responding prey's resource) of the prey (d) and with four links in which the predator affects a mutualist (i.e. consumes a competitor of the responding prey's resource) of the prey (e).
Figure 3. Example of a TMIE, DMIE and their interaction caused by a predator on a prey's competitor. A larval dragonfly predator reduces small tadpole density and induces a change in small tadpole foraging traits (habitat preference and activity levels). These two predator effects cause an increase in periphyton resource levels and large tadpole (competitor) growth. Combinations of treatments allowed teasing apart of the relative contributions of the TMIE and DMIE and their interaction. The DMIE was a small fraction of the total (net) effect of the predator, the TMIE was on the same order of magnitude as the DMIE, and there was a large interaction between the two effects. Reproduced from Peacor and Werner (2001). Copyright 2001, National Academy of Sciences, USA.
close
 References
    book Abrams PA (1987) "Indirect interactions between species that share a predator: varieties on a theme". In: Kerfoot WC and Sih A (eds) Predation: Direct and Indirect Impacts on Aquatic Communities, pp. 38–54. Hanover: University Press of New England.
    Abrams PA (1995) Implications of dynamically variable traits for identifying, classifying and measuring direct and indirect effects in ecological communities. American Naturalist 146: 112–134.
    Abrams PA (2007) Defining and measuring the impact of dynamic traits on interspecific interactions. Ecology 88: 2555–2562.
    book Abrams PA, Menge BA, Mittelbach GG, Spiller D and Yodzis P (1996) "The role of indirect effects in food webs". In: Polis G and Winemiller K (eds) Food Webs: Dynamics and Structure, pp. 371–395. New York: Chapman & Hall.
    Anholt BR and Werner EE (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology 76: 2230–2234.
    Bolker B, Holyoak M, Krivan V, Rowe L and Schmitz O (2003) Connecting theoretical and empirical studies of trait-mediated interactions. Ecology 84: 1101–1114.
    Bronmark C and Miner JG (1992) Predator-induced phenotypical change in body morphology in Crucian Carp. Science 258: 1348–1350.
    Byrnes J, Stachowicz JJ, Hultgren KM et al. (2006) Predator diversity strengthens trophic cascades in kelp forests by modifying herbivore behaviour. Ecology Letters 9: 61–71.
    Creel S and Christianson D (2008) Relationships between direct predation and risk effects. Trends in Ecology and Evolution 23: 194–201.
    Frid A, Baker GG and Dill LM (2006) Do resource declines increase predation rates on north pacific harbor seals? A behavior-based plausibility model. Marine Ecology-Progress Series 312: 265–275.
    Grabowski JH (2004) Habitat complexity disrupts predator-prey interactions but not the trophic cascade on oyster reefs. Ecology 85: 995–1004.
    Griffin CAM and Thaler JS (2006) Insect predators affect plant resistance via density- and trait-mediated indirect interactions. Ecology Letters 9: 335–343.
    Holker F and Mehner T (2005) Simulation of trait- and density-mediated indirect effects induced by piscivorous predators. Basic and Applied Ecology 6: 289–300.
    Krivan V (1998) Effects of optimal antipredator behavior of prey on predator–prey dynamics: role of refuges. Theoretical Population Biology 53: 131–142.
    Lass S and Spaak P (2003) Chemically induced anti-predator defences in plankton: a review. Hydrobiologia 491: 221–239.
    Lewin WC, Arlinghaus R and Mehner T (2006) Documented and potential biological impacts of recreational fishing: insights for management and conservation. Reviews in Fisheries Science 14: 305–367.
    Lima SL (1998) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Advances in the Study of Behavior 27: 215–290.
    Long JD, Hamilton RS and Mitchell JL (2007) Asymmetric competition via induced resistance: specialist herbivores indirectly suppress generalist preference and populations. Ecology 88: 1232–1240.
    Losey JE and Denno RF (1998) Positive predator–predator interactions: enhanced predation rates and synergistic suppression of aphid populations. Ecology 79: 2143–2152.
    Luttbeg B and Schmitz OJ (2000) Predator and prey models with flexible individual behavior and imperfect information. American Naturalist 155: 669–683.
    McIntosh AR and Townsend CR (1996) Interactions between fish, grazing invertebrates and algae in a New Zealand stream: a trophic cascade mediated by fish induced changes to grazer behavior? Oecologia 108: 174–181.
    McPeek MA and Peckarsky BL (1998) Life histories and the strengths of species interactions: combining mortality, growth, and fecundity effects. Ecology 79: 867–879.
    Miner BG, Sultan SE, Morgan SG, Padilla DK and Relyea RA (2005) Ecological consequences of phenotypic plasticity. Trends in Ecology & Evolution 20: 685–692.
    Nelson EH (2007) Predator avoidance behavior in the pea aphid: costs, frequency, and population consequences. Oecologia 151: 22–32.
    Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annual Review of Ecology Evolution and Systematics 36: 81–105.
    Pangle KL, Peacor SD and Johannsson OE (2007) Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88: 402–412.
    Peacor SD (2002) Positive effect of predators on prey growth rate through induced modifications of prey behaviour. Ecology Letters 5: 77–85.
    Peacor SD and Werner EE (2001) The contribution of trait-mediated indirect effects to the net effects of a predator. Proceedings of the National Academy of Sciences of the USA 98: 3904–3908.
    Peacor SD and Werner EE (2004a) How dependent are species-pair interaction strengths on other species in the food web? Ecology 85: 2754–2763.
    Peacor SD and Werner EE (2004b) Context dependence of nonlethal effects of a predator on prey growth. Israel Journal of Zoology 50: 139–167.
    Peckarsky BL, Cowan CA, Penton MA and Anderson C (1993) Sublethal consequences of stream-dwelling predatory stoneflies on mayfly growth and fecundity. Ecology 74: 1836–1846.
    Persson L and De Roos AM (2003) Adaptive habitat use in size-structured populations: linking individual behavior to population processes. Ecology 84: 1129–1139.
    Philpott SM, Maldonado J, Vandermeer J and Perfecto I (2004) Taking trophic cascades up a level: behaviorally modified effects of phorid flies on ants and ant prey in coffee agroecosystems. Oikos 105: 141–147.
    Preisser EL, Bolnick DI and Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86: 501–509.
    Relyea RA (2000) Trait-mediated indirect effects in larval anurans: reversing competition with the threat of predation. Ecology 81: 2278–2289.
    Ripple WJ and Beschta RL (2007) Restoring Yellowstone's aspen with wolves. Biological Conservation 138: 514–519.
    Schmitz OJ (2008) Effects of predator hunting mode on grassland ecosystem function. Science 319: 952–954.
    Schmitz OJ, Krivan V and Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecology Letters 7: 153–163.
    Soluk DA and Collins NC (1988) Synergistic interactions between fish and stoneflies: facilitation and interference among stream predators. Oikos 52: 94–100.
    van der Stap I, Vos M, Verschoor AM, Helmsing NR and Mooij WM (2007) Induced defenses in herbivores and plants differentially modulate a trophic cascade. Ecology 88: 2474–2481.
    book Tollrian R and Harvell CD (eds) (1999) The ecology and evolution of inducible defenses. New Jersey: Princeton University Press.
    Trussell GC, Ewanchuk PJ and Matassa CM (2006a) Habitat effects on the relative importance of trait- and density-mediated indirect interactions. Ecology Letters 9: 1245–1252.
    Trussell GC, Ewanchuk PJ and Matassa CM (2006b) The fear of being eaten reduces energy transfer in a simple food chain. Ecology 87: 2979–2984.
    Turner AM (1997) Contrasting short-term and long-term effects of predation risk on consumer habitat use and resources. Behavioral Ecology 8: 120–125.
    Turner AM (2004) Non-lethal effects of predators on prey growth rates depend on prey density and nutrient additions. Oikos 104: 561–569.
    Verschoor AM, Vos MM and van der Stap I (2004) Inducible defences prevent strong population fluctuations in bi- and tritrophic food chains. Ecology Letters 7: 1143–1148.
    Werner EE and Anholt BR (1996) Predator-induced behavioral indirect effects: consequences to competitive interactions in anuran larvae. Ecology 77: 157–169.
    Werner EE and Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84: 1083–1100.
    Werner EE and Peacor SD (2006) Lethal and nonlethal predator effects on an herbivore guild mediated by system productivity. Ecology 87: 347–361.
    Wirsing AJ, Heithaus MR and Dill LM (2007) Can you dig it? Use of excavation, a risky foraging tactic, by dugongs is sensitive to predation danger. Animal Behaviour 74: 1085–1091.
    Wootton JT (1993) Indirect effects and habitat use in an intertidal community: interaction chains and interaction modifications. American Naturalist 141: 71–98.
 Further Reading
    Abrams PA (1987) On classifying interactions between populations. Oecologia 73: 272–281.
    Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294: 321–326.
    Kareiva P (1994) Special feature: higher order interactions as a foil to reductionist ecology. Ecology 75: 1527–1528.
    book Polis GA and Winemiller KO (1996) Food Webs. New York: Chapman & Hall.
    Schmitz OJ, Adler FR and Agrawal AA (2003) Linking individual-scale trait plasticity to community dynamics. Ecology 84: 1081–1082.
    Vos M, Kooi BW, DeAngelis DL and Mooij WM (2004) Inducible defences and the paradox of enrichment. Oikos 105: 471–480.
    Werner EE (1992) Individual behavior and higher-order species interactions. American Naturalist 140: S5–S32.
    Wootton JT and Emmerson M (2005) Measurement of interaction strength in nature. Annual Review of Ecology Evolution and Systematics 36: 419–444.

Related Sub-Topics:

Herbivory, Predation and Parasitism | Community Structure
Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Nonconsumptive Effects of Predators and Trait‐Mediated Indirect Effects
 
How to Cite close
Peacor, Scott D, and Werner, Earl E(Dec 2008) Nonconsumptive Effects of Predators and Trait‐Mediated Indirect Effects. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021216]