Abstract
One of the classic ecological questions is how predators affect population size. This is often assessed by measuring how many individuals are killed by a predator, yet such direct effects may only be a relatively minor part of population dynamics. Predators frequently affect prey populations indirectly, with the fear of predation resulting in costly behavioural compensation that has the potential to lead to large population and community effects. Large observable lethal effects may then just represent the most easily observed “special” cases of the effects of predation on populations, with the costs of non-lethal effects being ubiquitous and usually dominant. This review explores these two ideas: that both cases where there are no population effects due to predation and those where lethal effects dominate are unusual and involve special circumstances. First, systems in which predation effects appear not to arise include (1) complete avoidance of predators by prey; (2) when other environmental factors limit populations so that predation is not additive to mortality; (3) when there are other more vulnerable prey for a predator; (4) when predators interact; (5) because the relationship of perceived predation risk with predator abundance is usually a non-linear function; (6) for the simple reason that non-lethal effects have not been considered. Second, lethal effects tend to dominate over non-lethal effects when (1) there is a high cost of compensating for predation risk associated with either a resource constraint or a particularly vulnerable niche or life-history stage (e.g. the nest stage generally for birds); (2) prey are the most popular prey of a predator or linear trophic chains operate; (3) there is evolutionary lag, such as introduced predators and naïve prey populations; (4) there are several predator species hunting the same prey in diverse ways. The presence of predators may or may not affect the size of a bird population at any particular life-history stage, although in most cases it will do so through non-lethal effects and, occasionally, through lethal effects. However, the presence of predators will always affect intra- and interspecific competition and so will always affect population dynamics. Studies that wish to fully demonstrate that predation has no effect on bird populations must show that lethal effects and the costs of non-lethal compensation by the prey do not significantly change its density and, consequently, the level of competition.
Similar content being viewed by others
References
Abrams PA (1984) Foraging time optimization and interactions in food webs. Am Nat 124:80–96
Abrams PA (1991) Strengths of indirect effects generated by optimal foraging. Oikos 62:167–176
Abrams PA (1993) Why predation rate should not be proportional to predator density. Ecology 74:726–733
Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326
Amar A, Redpath S, Sim I, Buchanan G (2010) Spatial and temporal associations between recovering populations of common raven Corvus corax and British upland wader populations. J Appl Ecol 47:253–262
Backman J, Alerstam T (2001) Confronting the winds: orientation and flight behaviour of roosting swifts, Apus apus. Proc R Soc Lond B 268:1081–1087
Balaz M, Weidinger K, Kocian L, Nemethova D (2007) Effect of habitat on blackcap, Sylvia atricapilla nest predation in the absence of corvid predators. Folia Zool 56:177–185
Bennett PM, Owens IPF (2002) Evolutionary ecology of birds: life histories, mating systems and extinction. Oxford University Press, Oxford
Blumstein DT, Daniel JC (2005) The loss of anti-predator behaviour following isolation on islands. Proc R Soc Lond B 272:1663–1668
Bolker B, Holyoak M, Krivan V, Rowe L, Schmitz O (2003) Connecting theoretical and empirical studies of trait-mediated interactions. Ecology 84:1101–1114
Bolnick DI, Preisser EL (2005) Resource competition modifies the strength of trait-mediated predator-prey interactions: a meta-analysis. Ecology 86:2771–2779
Bolton M, Tyler G, Smith K, Bamford R (2007) The impact of predator control on lapwing Vanellus vanellus breeding success on wet grassland nature reserves. J Appl Ecol 44:534–544
Bourne WRP (1960) A hunting partnership between two birds of prey. Ibis 102:136
Boyce MS, Sinclair ARE, White GC (1999) Seasonal compensation of predation and harvesting. Oikos 87:419–426
Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014
Brown JS, Laundre JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399
Butler SJ, Whittingham MJ, Quinn JL, Cresswell W (2005) Quantifying the interaction between food density and habitat structure in determining patch selection. Anim Behav 69:337–343
Caro TM (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago
Chase JM, Abrams PA, Grover JP, Diehl S, Chesson P, Holt RD, Richards SA, Nisbet RM, Case TJ (2002) The interaction between predation and competition: a review and synthesis. Ecol Lett 5:302–315
Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201
Cresswell W (1993) Escape responses by redshanks, Tringa totanus, on attack by avian predators. Anim Behav 46:609–611
Cresswell W (1994) Age-dependent choice of redshank (Tringa totanus) feeding location: profitability or risk? J Anim Ecol 63:589–600
Cresswell W (1995) Selection of avian prey by wintering sparrowhawks Accipiter nisus in southern Scotland. Ardea 83:381–389
Cresswell W (1996) Surprise as a winter hunting strategy in Sparrowhawks Accipiter nisus, Peregrines Falco peregrinus and Merlins F. columbarius. Ibis 138:684–692
Cresswell W (2008) Non-lethal effects of predation risk in birds. Ibis 150:3–17
Cresswell W, Whitfield DP (1994) The effects of raptor predation on wintering wader populations at the Tyninghame estuary, southeast Scotland. Ibis 136:223–232
Cresswell W, Whitfield DP (2008) How starvation risk in Redshanks results in predation mortality from Sparrowhawks. Ibis 150:209–218
Cresswell W, Holt S, Reid JM, Whitfield DP, Mellanby RJ, Norton DW, Waldron S (2004) The energetic costs of egg heating constrain incubation attendance but do not determine daily energy expenditure in the pectoral sandpiper. Behav Ecol 15:498–507
Cresswell W, Lind J, Quinn JL (2010) Predator hunting success and prey vulnerability: quantifying the spatial scale over which lethal and non-lethal effects of predation occur. J Anim Ecol 79:556–562
Crooks KR, Soule ME (1999) Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563–566
Dekker D (1998) Over-ocean flocking by Dunlins, Calidris alpina, and the effect of raptor predation at Boundary Bay, British Columbia. Can Field Nat 112:694–697
Diamond JM (1989) The present, past and future of human-caused extinctions. Philos Trans R Soc B 325:469–477
Dobson A, Power DM (1990) Survival rates and their relationship to life-history traits in some common British birds. Curr Ornithol 7:115–146
Dunnet GM, Ollason JC (1978) The estimation of survival rate in the fulmar, Fulmarus glacialis. J Anim Ecol 47:507–520
Duriez O, Fritz H, Binet F, Tremblay Y, Ferrand Y (2005) Individual activity rates in wintering Eurasian woodcocks: starvation versus predation risk trade-off? Anim Behav 69:39–49
Errington PL (1943) An analysis of mink predation upon muskrats in north-central United States. Iowa Agric Res Bull 320:798–924
Errington PL (1945) Some contributions of a fifteen-year study of the northern bobwhite to a knowledge of population phenomena. Ecol Monog 15:1–34
Evans KL (2004) The potential for interactions between predation and habitat change to cause population declines of farmland birds. Ibis 146:1–13
Facon B, Genton BJ, Shykoff J, Jarne P, Estoup A, David P (2006) A general eco-evolutionary framework for understanding bioinvasions. Trends Ecol Evol 21:130–135
Fletcher K, Aebischer NJ, Baines D, Foster R, Hoodless AN (2010) Changes in breeding success and abundance of ground-nesting moorland birds in relation to the experimental deployment of legal predator control. J Appl Ecol 47:263–272
Fontaine JJ, Martel M, Markland HA, Niklison AA, Decker KL, Martin TE (2007) Testing ecological and behavioral correlates of nest predation. Oikos 116:1887–1894
Gosler AG (1996) Environmental and social determinants of winter fat storage in the great tit Parus major. J Anim Ecol 65:1–17
Götmark F, Post P (1996) Prey selection by Sparrowhawks, Accipiter nisus - relative predation risk for breeding passerine birds in relation to their size, ecology and behavior. Philos Trans R Soc B 351:1559–1577
Grand TC (2002) Alternative forms of competition and predation dramatically affect habitat selection under foraging-predation-risk trade-offs. Behav Ecol 13:280–290
Green RE, Tyler GA, Stowe TJ, Newton AV (1997) A simulation model of the effect of mowing of agricultural grassland on the breeding success of the corncrake (Crex crex). J Zool 243:81–115
Hagelin JC (2003) A field study of ornaments, body size, and mating behavior of the Gambel’s Quail. Wilson Bull 115:246–257
Hanssen SA, Engebretsen H, Erikstad KE (2002) Incubation start and egg size in relation to body reserves in the common eider. Behav Ecol Sociobiol 52:282–288
Heithaus MR, Wirsing AJ, Burkholder D, Thomson J, Dill LM (2009) Towards a predictive framework for predator risk effects: the interaction of landscape features and prey escape tactics. J Anim Ecol 78:556–562
Holt RH, Davies ZG, Staddon S (2008) Meta-analysis of the effects of predation on animal prey abundance: evidence from UK vertebrates. PLoS ONE 3(6):e2400. doi:https://doi.org/10.1371/journal.pone.0002400
Houston AI, McNamara JM, Hutchinson JMC (1993) General results concerning the trade-off between gaining energy and avoiding predation. Philos Trans R Soc B 341:375–397
Igual JM, Forero MG, Gomez T, Oro D (2007) Can an introduced predator trigger an evolutionary trap in a colonial seabird? Biol Conserv 137:189–196
Inger R, Bearhop S, Robinson JA, Ruxton G (2006) Prey choice affects the trade-off balance between predation and starvation in an avian herbivore. Anim Behav 71:1335–1341
Inger R, Gudmundsson GA, Ruxton GD, Newton J, Colhoun K, Auhage S, Bearhop S (2008) Habitat utilisation during staging affects body condition in a long distance migrant, Branta bernicla hrota: potential impacts on fitness? J Avian Biol 39:704–708
Innes J, Kelly D, Overton JM, Gillies C (2010) Predation and other factors currently limiting New Zealand forest birds. NZ J Ecol 34:86–114
Jenkins D, Watson A, Miller GR (1964) Predation and red grouse populations. J Appl Ecol 1:183–195
Kotler BP, Blaustein L (1995) Titrating food and safety in a heterogeneous environment—when are the risky and safe patches of equal value. Oikos 74:251–258
Kotler BP, Blaustein L, Brown JS (1992) Predator facilitation—the combined effect of snakes and owls on the foraging behavior of gerbils. Ann Zool Fenn 29:199–206
Krebs CJ, Boutin S, Boonstra R, Sinclair ARE, Smith JNM, Dale MRT, Martin K, Turkington R (1995) Impact of food and predation on the snowshoe hare cycle. Science 269:1112–1115
Krivan V, Schmitz OJ (2004) Trait and density mediated indirect interactions in simple food webs. Oikos 107:239–250
Lack D (1954) The natural regulation of animal numbers. Clarendon, Oxford
Lack D (1956) Swifts in a tower. Methuen, London
Lank DB, Butler RW, Ireland J, Ydenberg RC (2003) Effects of predation danger on migration strategies of sandpipers. Oikos 103:303–319
Larsen T, Sordahl TA, Byrkjedal I (1996) Factors related to aggressive nest protection behaviour: a comparative study of Holarctic waders. Biol J Linn Soc 58:409–439
Lecomte VJ, Sorci G, Cornet S, Jaeger A, Faivre B, Arnoux E, Gaillard M, Trouve C, Besson D, Chastel O, Weimerskirch H (2010) Patterns of aging in the long-lived wandering albatross. Proc Natl Acad Sci USA 107:6370–6375
Leibold M (1991) Trophic interactions and habitat segregation between competing Daphnia species. Oecologia 86:510–520
Lessells CM, Krebs JR, Davies NB (1991). The evolution of life histories. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell Scientific, Oxford, pp 137–168
Letnic M, Koch F, Gordon C, Crowther MS, Dickman CR (2009) Keystone effects of an alien top-predator stem extinctions of native mammals. Proc R Soc Lond B 276:3249–3256
Lima SL (1986) Predation risk and unpredictable feeding conditions: determinants of body mass in birds. Ecology 67:377–385
Lima SL (1993) Ecological and evolutionary perspectives on escape from predatory attack—a survey of North-American birds. Wilson Bull 105:1–47
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
Lima SL (2002) Putting predators back into behavioral predator-prey interactions. Trends Ecol Evol 17:70–75
Lima SL (2009) Predators and the breeding bird: behavioral and reproductive flexibility under the risk of predation. Biol Rev 84:485–513
Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Lima SL, Mitchell WA, Roth TC (2003) Predators feeding on behaviourally responsive prey: some implications for classical models of optimal diet choice. Evol Ecol Res 5:1083–1102
Lingle S, Pellis SM, Wilson WF (2005) Interspecific variation in antipredator behaviour leads to differential vulnerability of mule deer and white-tailed deer fawns early in life. J Anim Ecol 74:1140–1149
Luttbeg B, Kerby JL (2005) Are scared prey as good as dead? Trends Ecol Evol 20:416–418
Luttbeg B, Rowe L, Mangel M (2003) Prey state and experimental design affect relative size of trait- and density-mediated indirect effects. Ecology 84:1140–1150
MacLeod R, Barnett P, Clark JA, Cresswell W (2005) Body mass change strategies in blackbirds Turdus merula: the starvation-predation risk trade-off. J Anim Ecol 74:292–302
Macleod R, Clark J, Cresswell W (2008) The starvation-predation risk trade-off, body mass and population status in the Common Starling Sturnus vulgaris. Ibis 150:199–208
Martin TE (1991) Food limitation in terrestrial breeding bird populations: is that all there is? Proc 20th Int Ornithol Congr 20:1595–1602
McGowan A, Cresswell W, Ruxton GD (2002) The effects of daily weather variation on foraging and responsiveness to disturbance in overwintering Red Knot (Calidris canutus). Ardea 90:229–237
McNamara JM, Houston AI (1987) Starvation and predation as factors limiting population size. Ecology 68:1515–1519
McNamara JM, Houston AI, Lima SL (1994) Foraging routines of small birds in winter: a theoretical investigation. J Avian Biol 25:287–302
Milinski M, Heller R (1978) The influence of a predator on optimal foraging behaviour of sticklebacks (Gasterosteus aculeatus L.). Nature 275:642–644
Newson SE, Rexstad EA, Baillie SR, Buckland ST, Aebischer NJ (2010) Population change of avian predators and grey squirrels in England: is there evidence for an impact on avian prey populations? J Appl Ecol 47:244–252
Newton I (1986) The Sparrowhawk. Poyser, Calton
Newton I (1993) Predation and limitation of bird numbers. Curr Ornithol 11:143–198
Newton I (1998) Population limitation in birds. Academic Press, London
Paclik M, Misik J, Weidinger K (2009) Nest predation and nest defence in European and North American woodpeckers: a review. Ann Zool Fenn 46:361–379
Page G, Whitacre DF (1975) Raptor predation on wintering shorebirds. Condor 77:73–83
Partridge L, Barton NH (1993) Optimality, mutation and the evolution of aging. Nature 362:305–311
Partridge L, Harvey PH (1988) The ecological context of life history evolution. Science 24:1449–1455
Peckarsky BL, McIntosh AR (1998) Fitness and community consequences of avoiding multiple predators. Oecologia 113:565–576
Peckarsky BL, Abrams PA, Bolnick DI, Dill LM, Grabowski JH, Luttbeg B, Orrock JL, Peacor SD, Preisser EL, Schmitz OJ, Trussell GC (2008) Revisiting the classics: considering nonconsumptive effects in textbook examples of predator-prey interactions. Ecology 89:2416–2425
Perez-Tris J, de la Puente J, Pinilla J, Bermejo A (2001) Body moult and autumn migration in the barn swallow Hirundo rustica: is there a cost of moulting late? Ann Zool Fenn 38:139–148
Perrins CM, Geer TA (1980) The effect of sparrowhawks on tit populations. Ardea 68:133–142
Pomeroy D (1990) Why fly? The possible benefits for lower mortality. Biol J Linn Soc 40:53–65
Pravosudov VV, Grubb TC, Nolan V Jr, Ketterson ED, Thompson CF (1997) Energy management in passerine birds during the nonbreeding season. Curr Ornithol 14:189–234
Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509
Preisser EL, Bolnick DI, Grabowski JH (2009) Resource dynamics influence the strength of non-consumptive predator effects on prey. Ecol Lett 12:315–323
Puigcerver M, Gallego S, Rodriguezteijeiro ID, Senar JC (1992) Survival and mean life span of the quail Coturnic c. coturnix. Bird Study 39:120–123
Redpath SM (1991) The impact of hen harriers on red grouse breeding success. J Appl Ecol 28:659–671
Redpath SM, Thirgood SJ, Leckie F (2001) Does supplementary feeding reduce predation of red grouse by hen harriers? J Appl Ecol 38:1157–1168
Ritchie EG, Johnson CN (2009) Predator interactions, mesopredator release and biodiversity conservation. Ecol Lett 12:982–998
Roth TC, Lima SL, Vetter WE (2006) Determinants of predation risk in small wintering birds: the hawk’s perspective. Behav Ecol Sociobiol 60:195–204
Salo P, Korpimaki E, Banks PB, Nordstrom M, Dickman CR (2007) Alien predators are more dangerous than native predators to prey populations. Proc R Soc Lond B 274:1237–1243
Schmidt-Wellenburg CA, Visser GH, Biebach B, Delhey K, Oltrogge M, Wittenzellner A, Biebach H, Kempenaers B (2008) Trade-off between migration and reproduction: does a high workload affect body condition and reproductive state? Behav Ecol 19:1351–1360
Schmitz OJ, Krivan V, Ovadia O (2004) Trophic cascades: the primacy of trait-mediated indirect interactions. Ecol Lett 7:153–163
Selas V (1993) Selection of prey by breeding Sparrowhawks Accipiter nisus in southern Norway: the importance of size and foraging behaviour of prey. Ornis Fenn 70:144–154
Sergio F, Hiraldo F (2008) Intraguild predation in raptor assemblages: a review. Ibis 150:132–145
Sih A (1980) Optimal behaviour: can foragers balance two conflicting demands. Science 210:1041–1043
Sih A (1982) Foraging strategies and the avoidance of predation by an aquatic insect Notonecta hoffmanni. Ecology 63:786–796
Sih A (1987) Prey refuges and predator-prey stability. Theor Popul Biol 31:1–12
Sih A, Christensen B (2001) Optimal diet theory: when does it work, and when and why does it fail? Anim Behav 61:379–390
Sih A, Bolnick DI, Luttbeg B, Orrock JL, Peacor SD, Pintor LM, Preisser E, Rehage JS, Vonesh JR (2010) Predator-prey naivete, antipredator behavior, and the ecology of predator invasions. Oikos 119:610–621
Smith RK, Pullin AS, Stewart GB, Sutherland WJ (2010) Effectiveness of predator removal for enhancing bird populations. Conserv Biol 24:820–829
Steadman DW (1995) Prehistoric extinction of Pacific island birds—biodiversity meets zooarchaeology. Science 267:1123–1131
Stillman RA, Goss-Custard JD (2002) Seasonal changes in the response of oystercatchers Haematopus ostralegus to human disturbance. J Avian Biol 33:358–365
Tharme AP, Green RE, Baines D, Bainbridge IP, O’Brien M (2001) The effect of management for red grouse shooting on the population density of breeding birds on heather-dominated moorland. J Appl Ecol 38:439–457
Tinbergen L (1946) Sperver als Roofvijand zan Zangvogels. Ardea 34:1–123
Tornberg R (1997) Prey selection of the goshawk Accipiter gentilis during the breeding season: the role of prey profitability and vulnerability. Ornis Fenn 74:15–28
Trussell GC, Ewanchuk PJ, Matassa CM (2006) Habitat effects on the relative importance of trait- and density-mediated indirect interactions. Ecol Lett 9:1245–1252
Tschanz B, Bersier LF, Bacher S (2007) Functional responses: a question of alternative prey and predator density. Ecology 88:1300–1308
van der Veen IT (2000) Daily routines and predator encounters in Yellowhammers Emberiza citrinella in the field during winter. Ibis 142:413–420
Videler JJ (2005) Avian flight. Oxford University Press, Oxford
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 76:211–221
Whittingham MJ, Evans KL (2004) The effects of habitat structure on predation risk in birds in agricultural landscapes. Ibis 146[Suppl 2]:210–220
Wirsing AJ, Cameron KE, Heithaus MR (2010) Spatial responses to predators vary with prey escape mode. Anim Behav 79:531–537
Yasue M, Quinn JL, Cresswell W (2003) Multiple effects of weather on the starvation and predation risk trade-off in choice of feeding location in redshanks. Funct Ecol 17:727–736
Ydenberg RC, Butler RW, Lank DB, Smith BD, Ireland J (2004) Western sandpipers have altered migration tactics as peregrine falcon populations have recovered. Proc R Soc Lond B 271:1263–1269
Zanette L, Smith JNM, van Oort H, Clinchy M (2003) Synergistic effects of food and predators on annual reproductive success in song sparrows. Proc R Soc Lond B 270:799–803
Zanette L, Clinchy M, Smith JNM (2006) Combined food and predator effects on songbird nest survival and annual reproductive success: results from a bi-factorial experiment. Oecologia 147:632–640
Acknowledgements
I thank Franz Barlein for inviting me to take part in the symposium to celebrate the 100th anniversary of IFV. I thank Ian Newton, Peter Becker and an anonymous referee for helpful comments on an earlier draft.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P. H. Becker.
Rights and permissions
About this article
Cite this article
Cresswell, W. Predation in bird populations. J Ornithol 152 (Suppl 1), 251–263 (2011). https://doi.org/10.1007/s10336-010-0638-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-010-0638-1