Abstract
Predation and predation risk have recently been shown to have profound effects on bird migration, but we still know relatively little about how birds respond to predation risk en route and how this is translated into fundamental aspects of optimal migration. Here, we make the case that to understand the fitness consequences of foraging and anti-predation behaviour en route we cannot rely on single behaviour relationships but must take many aspects of behaviour into account, because of predation risk compensation. We show this in a case study of fat and vigilant birds feeding close to cover, which emphasises the importance and potential of predation risk compensation. Another reason for taking many aspects of behaviour into account is that different behaviours need not contribute equally to individual fitness. Birds faced with an increased predation risk during migration can compensate for increased predation risk in different ways. This implies that the adaptive value of a behavioural trait can still be ambiguous even if a survival cost can be correlated with particular behaviour where all other things are equal (e.g. in an experiment). That is because in natural systems there may frequently be many other ways for animals to compensate, because all other things are never equal, so that the particular behaviour can actually be of little consequence to individual fitness. In conclusion, when studying foraging decisions and anti-predation behaviour during stopover potential compensatory mechanisms should be incorporated. This knowledge is also critical for improving future models of optimal migration.
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References
Anholt BR, Werner EE (1995) Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology 76:2230–2234
Biro PA, Post JR, Parkinson EA (2003) From individuals to populations: prey fish risk-taking mediates mortality in whole system experiments. Ecology 84:2419–2431
Blem CR (1975) Geographic variation in wing-loading of the house sparrow. Wilson Bull 87:543–549
Blums P, Clark RG (2004) Correlates of lifetime reproductive success in three species of European ducks. Oecologia 140:61–67
Burns JG, Ydenberg RC (2002) The effects of wing loading and gender on the escape flights of least sandpipers (Calidris minutilla) and western sandpipers (Calidris mauri). Behav Ecol Sociobiol 52:128–136
Carrascal LM, Polo V (1999) Coal tits, Parus ater, lose weight in response to chases by predators. Anim Behav 58:281–285
Cooper WE Jr, Vitt LJ, Hedges R, Huey RB (1990) Locomotor impairment and defense in gravid lizards (Eumeces laticeps): behavioral shift in activity may offset costs of reproduction in an active forager. Behav Ecol Sociobiol 27:153–157
Cresswell W (1994a) Age-dependent choice of redshank (Tringa totanus) feeding location: profitability or risk? J Anim Ecol 63:589–600
Cresswell W (1994b) Flocking is an effective anti-predation strategy in redshanks, Tringa totanus. Anim Behav 47:433–442
Downes SJ (2002) Size-dependent predation by snakes: selective foraging or differential prey vulnerability? Behav Ecol 13:551–560
Fitzgibbon CD (1989) A cost to individuals with reduced vigilance in groups of Thomson’s gazelles hunted by cheetahs. Anim Behav 37:508–510
Fransson T, Weber TP (1997) Migratory fuelling in blackcaps (Sylvia atricapilla) under perceived risk of predation. Behav Ecol Sociobiol 41:75–80
Gosler AG, Greenwood JJD, Perrins C (1995) Predation risk and the cost of being fat. Nature 377:621–623
Hinsley SA, Bellamy PE, Moss D (1995) Sparrowhawk Accipiter nisus predation and feeding site selection by tits. Ibis 137:418–420
Houston AI, Welton NJ, McNamara JM (1997) Acquisition and maintenance costs in the long-term regulation of avian fat reserves. Oikos 78:331–340
Kaby U, Lind J (2003) What limits predator detection in blue tits (Parus caeruleus): posture, task or orientation? Behav Ecol Sociobiol 54:534–538
Kenward RE (1978) Hawks and doves: factors affecting success and selection in goshawk attacks on woodpigeons. J Anim Ecol 47:449–460
Kullberg C, Fransson T, Jakobsson S (1996) Impaired predator evasion in fat blackcaps (Sylvia atricapilla). Proc R Soc Lond B 263:1671–1675
Kullberg C, Jakobsson S, Fransson T (2000) High migratory fuel loads impair predator evasion in sedge warblers. Auk 117:1034–1038
Lank DB, Butler RW, Ireland J, Ydenberg RC (2003) Effects of predation danger on migration strategies of sandpipers. Oikos 103:303–319
Lank DB, Ydenberg RC (2003) Death and danger at migratory stopovers: problems with “predation risk”. J Avian Biol 34:225–228
Lilliendahl K (1997) The effect of predator presence on body mass in captive greenfinches. Anim Behav 53:75–81
Lilliendahl K (1998) Yellowhammers get fatter in the presence of a predator. Anim Behav 55:1335–1340
Lima SL (1986) Predation risk and unpredictable feeding conditions: determinants of body mass in birds. Ecology 67:377–385
Lima SL (1998a) Nonlethal effects in the ecology of predator-prey interactions. Bioscience 48:25–34
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
Lind J (2004) What determines probability of surviving predator attacks in bird migration? The relative importance of vigilance and fuel load. J Theor Biol 231:223–227
Lind J, Fransson T, Jakobsson S, Kullberg C (1999) Reduced take-off ability in robins (Erithacus rubecula) due to migratory fuel load. Behav Ecol Sociobiol 46:65–70
Lind J, Jakobsson S (2001) Body building and concurrent mass loss: flight adaptations in tree sparrows. Proc R Soc Lond B 268:1915–1919
Lindström Å (1989) Finch flock size and risk of hawk predation at a migratory stopover site. Auk 106:225–232
Lindström Å (1990) The role of predation risk in stopover habitat selection in migrating bramblings, Fringilla montifringilla. Behav Ecol 1:102–105
Lindström Å, Kvist A, Piersma T, Dekinga A, Dietz MW (2000) Avian pectoral muscle size rapidly tracks body mass changes during flight, fasting and fuelling. J Exp Biol 203:913–919
Lindström Å, Rosén M (2002) The cost of avian winter stores: intra-individual variation in basal metabolic rate of a wintering passerine, the greenfinch Carduelis chloris. Avian Sci 2:139–144
Moore FR (1994) Resumption of feeding under risk of predation: effect of migratory condition. Anim Behav 48:975–977
Peacor SD, Werner EE (2001) The contribution of trait-mediated indirect effects to the net effects of a predator. Proc Natl Acad Sci 98:3904–3908
Pérez-Tris J, Díaz JA, Tellería JL (2004) The loss of body mass under risk of predation: cost of anti-predatory behaviour or adaptive fit-for-escape? Anim Behav 67:511–521
Piersma T, Koolhaas A, Jukema J (2003) Seasonal body mass changes in Eurasian golden plovers Pluvialis apricaria staging in the Netherlands: decline in late autumn mass peak correlates with increase in raptor numbers. Ibis 145:565–571
Pravosudov VV, Grubb TC Jr (1998) Management of fat reserves in tufted titmice Baelophus bicolor in relation to risk of predation. Anim Behav 56:49–54
Schmaljohann H, Dierschke V (2005) Optimal bird migration and predation risk: a field experiment with northern wheatears Oenanthe oenanthe. J Anim Ecol 74:131–138
Schwarzkopf L, Shine R (1992) Costs of reproduction in lizards: escape tactics and susceptibility to predation. Behav Ecol Sociobiol 31:17–25
Sih A (1986) Antipredator responses and the perception of danger by mosquito larvae. Ecology 67:434–441
Sillet TS, Holmes RT (2002) Variation in survivorship of a migratory songbird throughout its annual cycle. J Anim Ecol 71:296–308
van der Veen IT (1999) Effects of predation risk on diurnal mass dynamics and foraging routines of yellowhammers (Emberiza citrinella). Behav Ecol 10:545–551
Whitfield DP (2003) Redshank Tringa totanus flocking behaviour, distance from cover and vulnerability to sparrowhawk Accipiter nisus predation. J Avian Biol 34:163–169
Wisenden BD, Cline A, Sparkes TC (1999) Survival benefit to antipredator behavior in the amphipod Gammarus minus (Crustacea: Amphipoda) in response to injury-released chemical cues from conspecifics and heterospecifics. Ethology 105:407–414
Ydenberg RC, Butler RW, Lank DB, Guglielmo CG, Lemon M, Wolf N (2002) Trade-offs, condition dependence and stopover site selection by migrating sandpipers. J Avian Biol 33:47–55
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
Alerstam T, Lindström A (1990) Optimal bird migration: the relative importance of time, energy, and safety. In: Gwinner B (ed) Bird migration: the physiology and ecophysiology. Springer, Berlin Heidelberg New York, 331–351
Hedenström A, Alerstam T (1997) Optimum fuel loads in migratory birds: distinguishing between time and energy minimization. J Theor Biol 189:227–234
Acknowledgements
JL would like to thank Åke Lindström and Thord Fransson for many fruitful discussions on this topic over the years. Will Cresswell is a Royal Society University Research Fellow and JL was supported by the Swedish Research Council.
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Communicated by F. Bairlein
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Lind, J., Cresswell, W. Anti-predation behaviour during bird migration; the benefit of studying multiple behavioural dimensions. J Ornithol 147, 310–316 (2006). https://doi.org/10.1007/s10336-005-0051-3
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DOI: https://doi.org/10.1007/s10336-005-0051-3