Abstract
Both predation and individual variation in life history traits influence population dynamics. Recent results from laboratory predator–prey systems suggest that differences between individuals can also influence predator–prey dynamics when different genotypes experience different predation-associated mortalities. Despite the growing number of studies in this field, there is no synthesis identifying the overall importance of the interactions between predation and individual heterogeneity and their role in shaping the dynamics of free-ranging populations of vertebrates. We aim to fill this gap with a review that examines how individual variability in prey susceptibility, in predation costs, in predator selectivity, and in predatory performance, might influence prey population dynamics. Based on this review, it is clear that (1) predation risk and costs experienced by free-ranging prey are associated with their phenotypic attributes, (2) many generalist predator populations consist of individual specialists with part of the specialization associated with their phenotypes, and (3) a complete understanding of the population dynamic consequences of predation may require information on individual variability in prey selection and prey vulnerability. Altogether, this work (1) highlights the importance of maintaining long-term, detailed studies of individuals of both predators and prey in contrasting ecological conditions, and (2) advocates for a better use of available information to account for interactive effects between predators and their prey when modelling prey population dynamics.
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References
Abrams PA (1995) Implications of dynamically variable traits for identifying, classifying, and measuring direct and indirect effects in ecological communities. Am Nat 146:112–134
Adams LG, Singer FJ, Dale BW (1995) Caribou calf mortality in Denali National Park, Alaska. J Wildl Manage 59:584–594
Altendorf KB, Laundré JW, López Gonzales CA, Brown JS (2001) Assessing effects of predation risk on foraging behavior of mule deer. J Mamm 82:430–439
Andruskiw M, Fryxell JM, Thompson ID, Baker JA (2008) Habitat-mediated variation in predation risk by the American marten. Ecology 89:2273–2280
Bakker RT (1983) The deer flees, the wolf pursues: incongruities in predator-prey coevolution. In: Futuyama DJ, Slatkin M (eds) Coevolution. Sinauer, Sunderland, pp 350–382
Baldus RD (2006) A man-eating lion from Tanzania with a toothache. Eur J Wildl Res 52:59–62
Ben-David M, Flynn RW, Schell DM (1997) Annual and seasonal changes in diets of martens: evidence from stable isotope analysis. Oecologia 111:280–291
Berger J (2007) Fear, human shields and the redistribution of prey and predators in protected areas. Biol Lett 3:620–623
Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28
Bolnick DI, Svanbäck R, Araujo MS, Persson L (2007) Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proc Natl Acad Sci USA 104:10075–10079
Bonsall M (2003) The role of variability and risk on the persistence of shared-enemy, predator–prey assemblages. J Theor Biol 221:193–204
Bonsall MB, Hassell MP (2005) Understanding ecological concepts: the role of laboratory systems. Adv Ecol Res 37:1–36
Boon AK, Réale D, Boutin S (2008) Personality, habitat use, and their consequences for survival in North American squirrels. Oikos 117:1321–1328
Breitenmoser U (1998) Large predators in the Alps: the fall and rise of man’s competitors. Biol Cons 3:279–289
Bronikowski AM, Clark ME, Rodd FH, Reznick DN (2002) Population-dynamic consequences of predator-induced life history variation in the guppy. Ecology 83:2194–2204
Brown JS (1988) Patch use as an indicator of habitat preference, predation risk and competition. Beh Ecol Sociobiol 22:37–47
Cam E, Link WA, Cooch EG, Monnat JY, Danchin E (2002) Individual covariation in life-history traits: seeing the trees despite the forest. Am Nat 159:96–105
Carey HV, Moore P (1986) Foraging and predation risks in yellow bellied marmots. Am Midl Nat 116:267–275
Coltman DW, O’Donoghue P, Jorgenson JT, Hogg JT, Strobeck C, Festa-Bianchet M (2003) Undesirable evolutionary consequences of trophy hunting. Nature 426:655–658
Cooper A, Pettorelli N, Durant SM (2007) Large carnivore menus: factors affecting hunting decisions by cheetahs in the Serengeti. Anim Behav 73:651–659
Costa GC, Vitt LJ, Pianka ER, Mesquita DO, Colli GR (2008) Optimal foraging constrains macroecological patterns: body size and dietary niche breadth in lizards. Glob Ecol Biogeo 17:670–677
Costantini D, Casagrande S, Di Lieto G, Fanfani A, Dell’Omo G (2005) Consistent differences in feeding habits between neighbouring breeding kestrels. Behaviour 142:1409–1421
Coulson TH, Benton TG, Lundberg P, Dall SRX, Kendall BE, Gaillard J-M (2006) Estimating individual contributions to population growth: evolutionary fitness in ecological time. Proc R Soc B 273:547–555
Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201
Creel S, Creel NM (2002) The African wild dog: behaviour, ecology and conservation. Princeton University Press, Princeton
Creel S, Winnie J Jr, Maxwell B, Hamlin K, Creel M (2005) Elk alter habitat selection as an antipredator response to wolves. Ecology 86:3387–3397
Creel S, Christianson D, Liley S, Winnie J Jr (2007) Effects of predation risk on reproductive physiology and demography in elk. Science 315:960
Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739
Dewitt TJ, Sih A, Hucko JA (1999) Trait compensation and co-specialization in a freshwater snail: size, shape and anti-predator behaviour. Anim Behav 58:397–407
Durant SM (2000) Predator avoidance, breeding experience and reproductive success in endangered cheetahs. Anim Behav 60:121–130
Durant SM, Craft M, Foley C, Hampson K, Lobora A, Msuha M, Eblate E, Bukombe J, Mchetto J, Pettorelli N (2010) Does size matter? An investigation of habitat use across a carnivore assemblage in the Serengeti, Tanzania. J Anim Ecol 79:1012–1022
Estes JA, Riedman ML, Staedler MM, Tinker MT, Lyon BE (2003) Individual variation in prey selection by sea otters: patterns, causes and implications. J Anim Ecol 72:144–155
Festa-Bianchet M, Coulson TH, Gaillard J-M, Hogg JT, Pelletier F (2006) Stochastic predation events and population persistence in bighorn sheep. Proc R Soc B 273:1537–1543
Field I, Bradshaw C, van den Hoff J, Burton H, Hindell M (2007) Age-related shifts in the diet composition of southern elephant seals expand overall foraging niche. Mar Biol 150:1441–1452
Fievet V, Lhomme P, Outreman Y (2008) Predation risk cues associated with killed conspecifics affect the behavior and reproduction of prey animals. Oikos 117:1380–1385
Fisk DL, Latta LC, Knapp RA, Pfrender ME (2007) Rapid evolution in response to introduced predators. I. Rates and patterns of morphological and life-history trait divergence. BMC Evol Biol 7:22
Fitzgibbon CD (1990) Why do hunting cheetahs prefer male gazelles? Anim Behav 40:837–845
FitzGibbon CD, Fanshawe JH (1989) The condition and age of Thomson’s gazelles killed by cheetahs and wild dogs. J Zool Lond 218:99–107
Fortin D, Beyer HL, Boyce MS, Smith DW, Duchesne T, Mao JS (2005) Wolves influence elk movements: behaviour shapes a trophic cascade in Yellowstone National Park. Ecology 86:1320–1330
Fraser DF, Huntingford FA (1986) Feeding and avoiding predation hazard: the behavioural response of the prey. Ethology 73:56–68
Fryxell JM, Lundberg P (1994) Diet choice and predator–prey dynamics. Evol Ecol 8:407–421
Fryxell JM, Mosser A, Sinclair ARE, Packer C (2007) Group formation stabilizes predator–prey dynamics. Nature 449:1041–1043
Fussmann GF, Ellner SP, Hairston NG Jr, Jones LE, Shertzer KW, Yoshida T (2005) Ecological and evolutionary dynamics of experimental plankton communities. Adv Ecol Res 37:221–241
Gaillard J-M, Festa-Bianchet M, Yoccoz NG, Loison A, Toigo C (2000) Temporal variation in fitness components and population dynamics of large herbivores. Ann Rev Ecol Syst 31:367–393
Gaydos JK, Raverty S, Baird RW, Osborne RW (2005) Suspected surplus killing of harbour seal pups (Phoca vitulina) by killer whales (Orcinus orca). Northwest Nat 86:150–154
Gilliam JF, Fraser DF (1987) Habitat selection under predation hazard: test of a model with foraging minnows. Ecology 68:1856–1862
Hairston NG Jr, Ellner SP, Geber MA, Yoshida T, Fox JA (2005) Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 8:1114–1127
Hanski I, Saccheri I (2006) Molecular-level variation affects population growth in a butterfly metapopulation. PLoS Biol 4:e129. doi:10.1371/journal.pbio.0040129
Hebblewhite M, Merrill EH, McDonald TL (2005) Spatial decomposition of predation risk using resource selection functions: an example in a wolf/elk predator/prey system. Oikos 111:101–111
Holling CS (1959) The components of predation as revealed by a study of small mammal predation of the European Pine Sawfly. Can Entomol 91:293–320
Houston AI, McNamara JM, Hutchinson JMC (1993) General results concerning the trade-off between gaining energy and avoiding predation. Phil Trans R Soc Lond B 341:375–397
Husseman JS, Murray DL, Power G, Mack C, Wenger CR, Quigley H (2003) Assessing differential prey selection patterns between two sympatric large carnivores. Oikos 101:591–601
Jung RE (1992) Individual variation in fruit choice by American robins (Turdus migratorius). Auk 109:98–111
Karell P, Lehtosalo N, Pietiainen H, Brommer JE (2010) Ural owl predation on field voles and bank voles by size, sex and reproductive state. Ann Zool Fennici 47:90–98
Kelly MJ, Durant SD (2000) Viability of the serengeti cheetah population. Cons Biol 14:786–797
Krivan V, Eisner J (2003) Optimal foraging and predator–prey dynamics III. Theor Pop Biol 63:269–279
Kruger SC, Lawes MJ, Maddock AH (1999) Diet choice and capture success of wild dog in Hluhluwe-Umfolozi Park, South Africa. J Zool Lond 248:543–551
Kruuk H (1986) Interactions between Felidae and their prey species: a review. In: Miller SD, Everett DD (eds) Cats of the world: biology, conservation and management. National Widlife Federation, Washington, DC, pp 253–273
Kunert G, Weisser WW (2003) The interplay between density- and trait-mediated effects in predator–prey interactions: a case study in aphid wing polymorphism. Oecologia 135:304–312
Laundré JW, Hernandez L, Altendorf KB (2001) Wolves, elk and bison: re-establishing the “landscape of fear” in Yellowstone National Park, USA. Can J Zool 79:1401–1409
Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Lomnicki A (1988) Population ecology of individuals. Princeton University press, Princeton
Lopez P, Hawlena D, Polo V, Amo L, Martin J (2005) Sources of individual shy–bold variations in antipredator behaviour of male Iberian rock lizards. Anim Behav 69:1–9
Luttbeg B, Schmitz OJ (2000) Predator and prey models with flexible individual behavior and imperfect information. Am Nat 155:669–683
MacArthur RH, Pianka ER (1966) On the optimal use of a patchy environment. Am Nat 100:603–609
MacLeod R, Barnett P, Clark J, Cresswell W (2006) Mass-dependent predation risk as a mechanism for house sparrow declines? Biol Lett 2:43–46
MacNamara JM, Houston AI (1986) The common currency for behavioural decisions. Am Nat 127:358–378
MacNamara JM, Houston AI (1992) Risk-sensitive foraging: a review of the theory. Bull Math Biol 54:355–378
MacNulty DR, Smith DW, Vucetich JA, Mech LD, Stahler DR, Packer C (2009) Predatory senescence in ageing wolves. Ecol Lett 12:1347–1356
Magnhagen C (1991) Predation risk as a cost of reproduction. Tr Ecol Evol 6:183–186
Magurran AE (1999) The causes and consequences of geographic variation in antipredator behavior: perspectives from fish populations. In: Foster SA, Endler JA (eds) Geographic variation in behavior: perspectives on evolutionary mechanisms. Oxford University Press, New York, pp 139–163
Maniscalco JM, Matkin CO, Maldini D, Calkins D, Atkinson S (2007) Assessing killer whale predation on Steller sea lions from field observations in Kenai fjords, Alaska. Mar Mammal Sci 23:306–321
Messier F (1994) Ungulate population models with predation: a case study with the North American moose. Ecology 75:478–488
Mills MGL, Gorman ML (1997) Factors affecting the density and distribution of wild dogs in the Kruger National Park. Cons Biol 11:1397–1406
Murray DL (2002) Differential body condition and vulnerability to predation in snowshoe hares. J Anim Ecol 71:614–625
Nilsen EB, Pettersen T, Gundersen H, Milner JM, Mysterud A, Solberg EJ, Andreassen HP, Stenseth NC (2005) Moose harvesting strategies in the presence of wolves. J Anim Ecol 42:389–399
Nilsen EB, Milner-Gulland EJ, Schofield L, Mysterud A, Stenseth NC, Coulson TN (2007) Wolf introduction to Scotland: public attitudes and consequences for red deer management. Proc R Soc Lond B 274:995–1002
Nilsen EB, Gaillard J-M, Andersen R, Odden J, Delorme D, van Laere G, Linnell JDC (2009) A slow life in hell or a fast life in heaven: demographic analyses of contrasting roe deer populations. J Anim Ecol 78:585–594
Norrdahl K, Korpimaki E (1998) Does mobility or sex of voles affect risk of predation by mammalian predators? Ecology 79:226–232
Nussey DH, Coulson TN, Festa-Bianchet M, Gaillard J-M (2008) Measuring senescence in wild animal populations: towards a longitudinal approach. Funct Ecol 22:393–406
Okuyama T (2008) Individual behavioural variation in predator–prey models. Ecol Res 23:665–671
Olito C, Fukami T (2009) Long-term effects of predator arrival timing on prey community succession. Am Nat 173:354–362
Ozoga JJ, Verme LJ (1986) Relation of maternal age to fawn-rearing success in white-tailed deer. J Wildl Manage 50:480–486
Packer C, Scheel D, Pusey AE (1990) Why lions form groups: food is not enough. Am Nat 136:1–19
Panzacchi M, Linnell JDC, Odden J, Andersen R (2008) When a generalist becomes a specialist: patterns of red fox predation on roe deer fawns under contrasting conditions. Can J Zool 86:116–126
Peacor SD (2002) Positive effect of predators on prey growth rate through induced modifications of prey behaviour. Ecol Lett 5:77–85
Pelletier F, Clutton-Brock TH, Pemberton J, Tuljapurkar S, Coulson TH (2007) The evolutionary demography of ecological change: linking trait variation and population growth. Science 315:1571–1574
Persson L, Anderson J, Wahlstrom E, Eklov P (1996) Size-specific interactions in lake systems: predator gape limitation and prey growth rate and mortality. Ecology 77:900–911
Pierce BM, Bleich VC, Bowyer RT (2000) Selection of mule deer by mountain lions and coyotes: effects of hunting style, body size, and reproductive status. J Mamm 81:462–472
Pole A, Gordon IJ, Gorman ML, MacAskill M (2004) Prey selection by African wild dogs (Lycaon pictus) in southern Zimbabwe. J Zool Lond 262:207–215
Post E, Peterson RO, Stenseth NC, McLaren BE (1999) Ecosystem consequences of wolf behavioural response to climate. Nature 401:905–907
Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86:501–509
Price T (1987) Diet variation in a population of Darwin’s finches. Ecology 68:1015–1028
Radloff FGT, du Toit JT (2004) Large predators and their prey in a southern African savanna: a predator’s size determines its prey size range. J Anim Ecol 73:410–423
Raia P, Meiri S (2006) The island rule in large mammals: paleontology meets ecology. Evolution 60:1731–1742
Réale D, Festa-Bianchet M (2003) Predator-induced natural selection on temperament in bighorn ewes. Anim Behav 65:463–470
Relyea RA (2002) The many faces of predation: how induction, selection, and thinning combine to alter prey phenotypes. Ecology 83:1953–1964
Relyea RA (2003) Predators come and predators go: the reversibility of predator-induced traits. Ecology 84:1840–1848
Reznick DA, Bryga H, Endler JA (1990) Experimentally induced life-history evolution in a natural population. Nature 346:357–359
Robinson HS, Wielgus RB, Cooley HS, Cooley SW (2008) Sink populations in carnivore management: cougar demography and immigration in a hunted population. Ecol Appl 18:1028–1037
Ross PI, Jalkotzy MG, Festa-Bianchet M (1997) Cougar predation on bighorn sheep in southwestern Alberta during winter. Can J Zool 74:771–775
Rutz C, Whittingham MJ, Newton I (2006) Age-dependent diet choice in an avian top predator. Proc Roy Soc Lond B 273:579–586
Saulitis E, Matkin C, Barrett-Lennard L, Heise K, Ellis G (2000) Foraging strategies of sympatric killer whale populations in Prince William Sound, Alaska. Mar Mammal Sci 16:94–109
Scheel D, Packer C (1991) Group hunting behaviour of lions: a search for cooperation. Anim Behav 41:697–709
Schmitz OJ (1998) Direct and indirect effects of predation and predation risk in old-field interaction webs. Am Nat 151:327–342
Shine R, Ambariyanto, Harlow PS, Mumpuni (1998) Ecological divergence among sympatric colour morphs in blood pythons, Python brongersmai. Oecologia 116:113–119
Sih A, Bell AM, Johnson JC (2004a) Behavioural syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378
Sih A, Bell AM, Johnson JC, Ziemba RE (2004b) Behavioural syndromes: an integrative overview. Quart Rev Biol 79:241–277
Sinclair ARE, Mduma SAR, Brashares JS (2003) Patterns of predation in a diverse predator–prey system. Nature 425:288–290
Stenseth NC, Falck W, Bjørnstad ON, Krebs CJ (1997) Population regulation in snowshoe hare and Canadian lynx: asymmetric food web configurations between hare and lynx. Proc Nat Acad Sci USA 94:5147–5152
Stewart DC, Middlemas SJ, Gardiner WR, Mackay S, Armstrong JD (2005) Diet and prey selection of cormorants (Phalacrocorax carbo) at Loch Leven, a major stocked trout fishery. J Zool (Lond) 267:191–201
Sutherland WJ, Ens BJ, Goss-Custard JD, Hulscher JB (1996) Specialization. In: Goss-Custard JD (ed) The oystercatcher. Oxford University Press, New York, pp 105–132
Svanback R, Bolnick DI (2007) Intraspecific competition drives increased resource use diversity within a natural population. Proc R Soc Lond 274:839–844
Svanback R, Persson L (2004) Individual diet specialization, niche width and population dynamics: implications for trophic polymorphisms. J Anim Ecol 73:973–982
Thompson ID, Peterson R (1988) Does wolf predation alone limit the moose population in Puskakwa park? J Wildl Manage 52:556–559
Turner JW Jr, Morrison ML (2001) Influence of predation by mountain lions on numbers and survivorship of a feral horse population. Southwest Nat 46:183–190
Unger PA, Lewis WM Jr (1983) Selective predation with respect to body size in a population of the fish Xenomelaniris venezuelae (Atherinidae). Ecology 64:1136–1144
Urban MC (2007) The growth-predation risk trade-off under a growing gape-limited predation threat. Ecology 88:2587–2597
Valière N, Fumagalli L, Gielly L, Miquel C, Lequette B, Poulle M-L, Weber J-M, Arlettaz R, Taberlet P (2003) Long-distance wolf recolonization of France and Switzerland inferred from non-invasive genetic sampling over a period of 10 years. Anim Cons 6:83–92
Verbeeck MEM, Boon A, Drent PJ (1996) Exploration, aggressive behaviour and dominance in pair-wise confrontations of juvenile male great tits. Behaviour 133:945–963
Vucetich JA, Smith DW, Stahler DR (2005) Influence of harvest, climate and wolf predation on Yellowstone elk, 1961–2004. Oikos 111:259–270
Wasserman SS, Mitter C (2008) The relationship of body size to breadth of diet in some Lepidoptera. Ecol Entomol 3:155–160
Webb JK, Shine R (1993) Prey-size selection, gape limitation and predator vulnerability in Australian blindsnakes. Anim Behav 45:1117–1126
Werner EE, Hall DJ (1974) Optimal foraging and the size selection of prey by the bluegill sunfish. Ecology 55:1042–1052
Winnie J, Creel S (2007) Sex-specific behavioural responses of elk to spatial and temporal variation in the threat of wolf predation. Anim Behav 73:215–225
Wittmer HU, Sinclair ARE, McLellan BN (2005) The role of predation in the decline and extirpation of woodland caribou populations. Oecologia 144:257–267
Wright RG (1999) Wildlife management in the national parks: questions in search of answers. Ecol Appl 9:30–36
Wright GJ, Peterson RO, Smith DW, Lemke TO (2006) Selection of northern Yellowstone elk by gray wolves and hunters. J Wildl Manage 70:1070–1078
Yoshida T, Jones LE, Ellner SP, Fussmann GF, Hairston NG (2003) Rapid evolution drives ecological dynamics in a predator–prey system. Nature 424:303–306
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Special thanks to Guy Cowlishaw for ideas, comments and suggestions on previous drafts of this work.
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Pettorelli, N., Coulson, T., Durant, S.M. et al. Predation, individual variability and vertebrate population dynamics. Oecologia 167, 305–314 (2011). https://doi.org/10.1007/s00442-011-2069-y
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DOI: https://doi.org/10.1007/s00442-011-2069-y