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Predation risk tradeoffs in prey: effects on energy and behaviour

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Abstract

The complexity of behavioural interactions in predator-prey systems has recently begun to capture trait-effects, or non-lethal effects, of predators on prey via induced behavioural changes. Non-lethal predation effects play crucial roles in shaping population and community dynamics, particularly by inducing changes to foraging, movement and reproductive behaviours of prey. Prey exhibit trade-offs in behaviours while minimizing predation risk. We use a novel evolutionary ecosystem simulation EcoSim to study such behavioural interactions and their effects on prey populations, thereby addressing the need for integrating multiple layers of complexity in behavioural ecology. EcoSim allows complex intra- and inter-specific interactions between behaviourally and genetically unique individuals called predators and prey, as well as complex predator-prey dynamics and coevolution in a tri-trophic and spatially heterogeneous world. We investigated the effects of predation risk on prey energy budgets and fitness. Results revealed that energy budgets, life history traits, allocation of energy to movements and fitness-related actions differed greatly between prey subjected to low-predation risk and high-predation risk. High-predation risk suppressed prey foraging activity, increased total movement and decreased reproduction relative to low-risk. We show that predation risk alone induces behavioural changes in prey which drastically affect population and community dynamics, and when interpreted within the evolutionary context of our simulation indicate that genetic changes accompanying coevolution have long-term effects on prey adaptability to the absence of predators.

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Notes

  1. http://sites.google.com/site/ecosimgroup/research/ecosystem-simulation

References

  • Abrams P, Matsuda H (1993) Effects of adaptive predatory and anti-predator behaviour in a two-prey one-predator system. Evol Ecol 7(3):312–326

    Article  Google Scholar 

  • Abrams PA (1987) The nonlinearity of competitive effects in models of competition for essential resources. Theor Popul Biol 32(1):50–65

    Article  Google Scholar 

  • Abrams PA (2000) The evolution of predator-prey interactions: theory and evidence. Annual Review of Ecology and Systematics:79–105

  • Abrams PA (2007) Habitat choice in predator-prey systems: spatial instability due to interacting adaptive movements. Am Nat 169(5):581–594

    Article  PubMed  Google Scholar 

  • Anholt BR, Werner EE (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology:2230–2234

  • Barry MJ (1994) The costs of crest induction for daphnia carinata. Oecologia 97(2):278–288

    Article  Google Scholar 

  • Biro PA, Post JR, Parkinson EA (2003) Population consequences of a predator-induced habitat shift by trout in whole-lake experiments. Ecology 84(3):691–700

    Article  Google Scholar 

  • Bolker B, Holyoak M, Krivan V, Rowe L, Schmitz O (2003) Connecting theoretical and empirical studies of trait-mediated interactions. Ecology 84(5):1101–1114

    Article  Google Scholar 

  • Brown JS (1999) Vigilance, patch use and habitat selection: foraging under predation risk. Evol Ecol Res 1 (1):49–71

  • Brown JS, Laundré JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. Journal of Mammalogy:385–399

  • Candolin U (1998) Reproduction under predation risk and the trade–off between current and future reproduction in the threespine stickleback. Proceedings of the Royal Society of London. Ser B: Biol Sci 265(1402):1171–1175

    Google Scholar 

  • Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23(4):194–201

    Article  PubMed  Google Scholar 

  • Creel S, Winnie J, Maxwell B, Hamlin K, Creel M (2005) Elk alter habitat selection as an antipredator response to wolves. Ecology 86(12):3387–3397

    Article  Google Scholar 

  • Cressman R, Kṙivan V, Garay J (2004) Ideal free distributions, evolutionary games, and population dynamics in multiple-species environments. Am Nat 164(4):473–489

    Article  PubMed  Google Scholar 

  • Cresswell W (2008) Non-lethal effects of predation in birds. Ibis 150(1):3–17

  • DeAngelis DL, Mooij WM (2005) Individual-based modeling of ecological and evolutionary processes. Annual Review of Ecology Evolution, and Systematics:147–168

  • Dill LM (1987) Animal decision making and its ecological consequences: the future of aquatic ecology and behaviour. Can J Zool 65(4):803–811

    Article  Google Scholar 

  • Downes S (2001) Trading heat and food for safety: costs of predator avoidance in a lizard. Ecology 82 (10):2870–2881

    Article  Google Scholar 

  • Edmunds M (1974) Defence in animals: a survey of anti-predator defences. Longman Harlow

  • Ferrari MC, Sih A, Chivers DP (2009) The paradox of risk allocation: a review and prospectus. Anim Behav 78(3):579–585

    Article  Google Scholar 

  • Fraser DF, Gilliam JF (1992) Nonlethal impacts of predator invasion: facultative suppression of growth and reproduction. Ecology 73(3):959–970

  • Fryxell JM, Greever J, Sinclair A (1988) Why are migratory ungulates so abundant American Naturalist:781–798

  • Fryxell JM, Mosser A, Sinclair AR, Packer C (2007) Group formation stabilizes predator–prey dynamics. Nature 449(7165):1041–1043

  • Giske J, Eliassen S, Fiksen Ø, Jakobsen PJ, Aksnes DL, Jørgensen C, Mangel M (2013) Effects of the emotion system on adaptive behavior. Am Nat 182(6):689–703

    Article  PubMed  Google Scholar 

  • Golestani A, Gras R (2010) Regularity analysis of an individual-based ecosystem simulation. Chaos: An Interdiscip J Nonlinear Sci 043120(4)

  • Gras R, Devaurs D, Wozniak A, Aspinall A (2009) An individual-based evolving predator-prey ecosystem simulation using fuzzy cognitive map as behavior model. Artif Life 15(4):423–463

    Article  PubMed  Google Scholar 

  • Grimm V (2005) Railsback, S. Individual-based modeling and ecology. Princeton university press, F.

    Google Scholar 

  • Hammond JI, Luttbeg B, Sih A (2007) Predator and prey space use: dragonflies and tadpoles in an interactive game. Ecology 88(6):1525–1535

    Article  PubMed  Google Scholar 

  • Harvey PH, Greenwood PJ (1978) Anti-predator defence strategies: some evolutionary problems. Behavioural Ecology:129–151

  • Hebblewhite M, Merrill EH (2007) Multiscale wolf predation risk for elk: does migration reduce risk Oecologia 152(2):377–387

    Article  PubMed  Google Scholar 

  • Hebblewhite M, Merrill EH (2009) Trade-offs between predation risk and forage differ between migrant strategies in a migratory ungulate. Ecology 90(12):3445–3454

    Article  PubMed  Google Scholar 

  • Hugie DM, Dill LM (1994) Fish and game: a game theoretic approach to habitat selection by predators and prey*. J Fish Biol 45(sA):151–169

    Article  Google Scholar 

  • Ives AR, Dobson AP (1987) Antipredator behavior and the population dynamics of simple predator-prey systems. The American Naturalist:431–447

  • Khater M, Gras R (2012) Adaptation and genomic evolution in ecosim. Proc Anim Animats 12:219–229

    Article  Google Scholar 

  • Khater M, Murariu D, Gras R (2014) Contemporary evolution and genetic change of prey as a response to predator removal. Ecol Inf 22:13–22

    Article  Google Scholar 

  • Kim S-H, Tschirhart J, Buskirk SW (2007) Reconstructing past population processes with general equilibrium models: house mice in kern county, california, 1926–1927. Ecol Modell 209(2):235–248

    Article  Google Scholar 

  • Korpimaki E, Norrdahl K, Valkama J (1994) Reproductive investment under fluctuating predation risk: microtine rodents and small mustelids. Evol Ecol 8(4):357–368

    Article  Google Scholar 

  • Kosko B (1986) Fuzzy cognitive maps. International Journal of Man-Machine Studies:65–75

  • Krebs CJ, Boutin S, Boonstra R, Sinclair A, Smith J, Dale MR, Martin K, Turkington R (1995) Impact of food and predation on the snowshoe hare cycle. Science 269(5227):1112–1115

    Article  CAS  PubMed  Google Scholar 

  • Krivan V (2003) Competitive co-existence caused by adaptive predators. Evol Ecol Res 5(8):1163–1182

    Google Scholar 

  • Kṙivan V (2007) The lotka-volterra predator-prey model with foraging–predation risk trade-offs. Am Nat 170(5):771–782

    Article  PubMed  Google Scholar 

  • Kṙivan V, Cressman R (2009) On evolutionary stability in predator-prey models with fast behavioral dynamics. Evolutionary Ecology Research:227–251

  • Kṙivan V, Schmitz OJ (2004) Trait and density mediated indirect interactions in simple food webs. Oikos 107(2):239–250

    Article  Google Scholar 

  • Lemon WC (1991) Fitness consequences of foraging behaviour in the zebra finch. Nature 352(6331):153–155

    Article  Google Scholar 

  • Lima SL (1998a) Nonlethal effects in the ecology of predator-prey interactions. Bioscience:25–34

  • Lima SL (1998b) Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. Adv Study Behav 27:215–290

  • Lima SL (2002) Putting predators back into behavioral predator–prey interactions. Trends Ecol Evol 17 (2):70–75

    Article  Google Scholar 

  • Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153(6):649–659

    Article  Google Scholar 

  • Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68(4):619–640

    Article  Google Scholar 

  • Lind J, Cresswell W (2005) Determining the fitness consequences of antipredation behavior. Behav Ecol 16(5):945–956

    Article  Google Scholar 

  • Luttbeg B, Kerby JL (2005) Are scared prey as good as dead Trends Ecol Evol 20(8):416–418

    Article  PubMed  Google Scholar 

  • Luttbeg B, Schmitz OJ (2000) Predator and prey models with flexible individual behavior and imperfect information. Am Nat 155(5):669–683

    Article  PubMed  Google Scholar 

  • Luttbeg B, Trussell GC (2013) How the informational environment shapes how prey estimate predation risk and the resulting indirect effects of predators. Am Nat 181(2):182–194

    Article  PubMed  Google Scholar 

  • Magnhagen C (1990) Reproduction under predation risk in the sand goby, pomatoschistus minutes, and the black goby, gobius niger: the effect of age and longevity. Behav Ecol Sociobiol 26(5):331–335

    Article  Google Scholar 

  • McCauley SJ, Rowe L (2010) Notonecta exhibit threat-sensitive, predator-induced dispersal. Biology Letters:449–452

  • McNamara JM, Houston AI (1986) The common currency for behavioral decisions. The American Naturalist:358–378

  • Morris DW (1987) Ecological scale and habitat use. Ecology 68(2):362–369

    Article  Google Scholar 

  • Peacor SD, Allesina S, Riolo RL, Hunter TS (2007) A new computational system, DOVE (Digital Organisms in a virtual Ecosystem), to study phenotypic plasticity and its effects in food webs. Ecol Modell 205 (1):13–28

    Article  Google Scholar 

  • Peacor SD, Werner EE (2004) How dependent are species-pair interaction strengths on other species in the food web Ecology 85(10):2754–2763

    Article  Google Scholar 

  • Peckarsky BL, Cowan CA, Penton MA, Anderson C (1993) Sublethal consequences of stream-dwelling predatory stoneflies on mayfly growth and fecundity. Ecology 74(6):1836–1846

    Article  Google Scholar 

  • Pelletier F, Garant D, Hendry AP (2009) Eco-evolutionary dynamics. Philos Trans Royal Soc B: Biol Sci 364(1523):1483–1489

    Article  CAS  Google Scholar 

  • Preisser EL, Bolnick DI (2008) The many faces of fear: comparing the pathways and impacts of nonconsumptive predator effects on prey populations. PLoS One 3(6):e2465

    Article  PubMed  PubMed Central  Google Scholar 

  • Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? the effects of intimidation and consumption in predator-prey interactions. Ecology 86(2):501–509

    Article  Google Scholar 

  • Ripple WJ, Beschta RL (2004) Wolves and the ecology of fear: can predation risk structure ecosystems BioScience 54 (8):755–766

    Article  Google Scholar 

  • Russell RW, Hunt GL, Coyle KO, Cooney RT (1992) Foraging in a fractal environment: spatial patterns in a marine predator-prey system. Landsc Ecol 7(3):195–209

    Article  Google Scholar 

  • Schmidt KA, Dall SR, Van Gils JA (2010) The ecology of information: an overview on the ecological significance of making informed decisions. Oikos 119(2):304–316

    Article  Google Scholar 

  • Schmitz OJ (2000) Combining field experiments and individual-based modeling to identify the dynamically relevant organizational scale in a field system. Oikos 89(3):471–484

    Article  Google Scholar 

  • Schmitz OJ, Booth G (1997) Modelling food web complexity: the consequences of individual-based, spatially explicit behavioural ecology on trophic interactions. Evol Ecol 11(4):379–398

    Article  Google Scholar 

  • Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7 (2):153–163

    Article  Google Scholar 

  • Schoener TW (1968) Optimal size and specialization in constant and fluctuating environments: an energy-time approach. In: Brookhaven Symposia in Biology, vol 22, pp 103–114

  • Schoener TW (1971) Theory of feeding strategies. Ann Rev Ecol Syst 2:369–404

    Article  Google Scholar 

  • Sih A (1987) Predators and prey lifestyles: an evolutionary and ecological overview. Predation: Direct and Indirect Impacts on Aquatic Communities:203–224

  • Skelly DK (1994) Activity level and the susceptibility of anuran larvae to predation. Anim Behav 47(2):465–468

    Article  Google Scholar 

  • Smith M (1991) Using massively-parallel supercomputers to model stochastic spatial predator-prey systems. Ecol Modell 58(1):347–367

    Article  Google Scholar 

  • Strand E, Huse G, Giske J (2002) Artificial evolution of life history and behavior. Am Nat 159(6):624–644

    Article  PubMed  Google Scholar 

  • Trussell GC, Ewanchuk PJ, Matassa CM (2006) The fear of being eaten reduces energy transfer in a simple food chain. Ecology 87(12):2979–2984

    Article  PubMed  Google Scholar 

  • Trussell GC, Matassa CM, Luttbeg B (2011) The effects of variable predation risk on foraging and growth: Less risk is not necessarily better. Ecology 92(9):1799–1806

    Article  PubMed  Google Scholar 

  • Tschirhart J (2004) A new adaptive system approach to predator–prey modeling. Ecol Modell 176(3):255–276

    Article  Google Scholar 

  • Valone TJ, Brown JS (1989) Measuring patch assessment abilities of desert granivores. Ecology:1800–1810

  • van Baalen M, Kṙivan V, Van Rijn PC, Sabelis MW (2001) Alternative food, switching predators, and the persistence of predator-prey systems. Am Nat 157(5):512–524

    Article  CAS  PubMed  Google Scholar 

  • Verdolin JL (2006) Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behav Ecol Sociobiol 60(4):457–464

    Article  Google Scholar 

  • Watson M, Aebischer NJ, Cresswell W (2007) Vigilance and fitness in grey partridges Perdix perdix: the effects of group size and foraging-vigilance trade-offs on predation mortality. J Anim Ecol 76(2):211–221

    Article  PubMed  Google Scholar 

  • Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84(5):1083–1100

    Article  Google Scholar 

  • Wirsing AJ, Cameron KE, Heithaus MR (2010) Spatial responses to predators vary with prey escape mode. Anim Behav 79(3):531–537

    Article  Google Scholar 

  • Wisenden BD (1993) Female convict cichlids adjust gonadal investment in current reproduction in response to relative risk of brood predation. Can J Zool 71(2):252–256

    Article  Google Scholar 

  • Wooster D, Sih A (1995) A review of the drift and activity responses of stream prey to predator presence. Oikos:3–8

  • Ylönen H (1994) Vole cycles and antipredatory behaviour. Trends Ecol Evol 9(11):426–430

    Article  PubMed  Google Scholar 

  • Yoshida T, Jones LE, Ellner SP, Fussmann GF, Hairston NG (2003) Rapid evolution drives ecological dynamics in a predator–prey system. Nature 424(6946):303–306

    Article  CAS  PubMed  Google Scholar 

  • Zanette LY, White AF, Allen MC, Clinchy M (2011) Perceived predation risk reduces the number of offspring songbirds produce per year. Science 334(6061):1398–1401

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work is supported by the NSERC grant ORGPIN 341854, the CRC grant 950-2-3617 and the CFI grant 203617 and is made possible by the facilities of the Shared Hierarchical Academic Research Computing Network (SHARCNET:www.sharcnet.ca).

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Authors and Affiliations

  1. School of Computer Science, University of Windsor, 401 Sunset Avenue, Windsor, ON, Canada

    Marwa Khater

  2. Department of Biology, University of Windsor, 401 Sunset Avenue, Windsor, ON, Canada

    Dorian Murariu

  3. School of Computer Science, Department of Biology University of Windsor, 401 Sunset Avenue, Windsor, Canada

    Robin Gras

  4. Great Lake Institute for Environmental Research, University of Windsor, Windsor, Canada

    Robin Gras

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  1. Marwa Khater
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Correspondence to Marwa Khater.

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Khater, M., Murariu, D. & Gras, R. Predation risk tradeoffs in prey: effects on energy and behaviour. Theor Ecol 9, 251–268 (2016). https://doi.org/10.1007/s12080-015-0277-5

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