Abstract
Habituation to nonlethal predation stimuli may provide benefits for animals living in areas with frequent encounters with low-risk predators. On the other hand, individuals can be very consistent in their antipredator responses, with shy individuals showing greater degree of responsiveness than bold individuals. However, the link between habituation or boldness and individual benefits has not been thoroughly investigated. We established whether and how two behavioral components associated with antipredator responses (habituation and boldness, and their interaction) would influence body condition, which is a parameter related to fitness. We conducted an outdoor semi-natural experiment with Iberian wall lizards (Podarcis hispanica). Individual boldness was consistent across contexts, but we did not find any effect of boldness or the interaction between boldness and habituation on body condition. However, those individuals that habituated more readily to a frequent predatory stimulus were able to increase their body condition more relative to lizards that habituated less. This finding highlights the importance of individual differences in behavioral plasticity, which could influence traits related to fitness. Habituation can provide benefits for individuals exposed to low-risk predators; however, individuals more prone to habituation could also experience mortality costs by wrongly habituating to a dangerous predator.
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References
Amo L, López P, Martín J (2006) Nature-based tourism as a form of predation risk affects body condition and health state of Podarcis muralis lizards. Biol Conserv 131:402–409
Amo L, López P, Martín J (2007) Refuge use: a conflict between avoiding predation and losing mass in lizards. Physiol Behav 90:334–343
Beale C, Monaghan P (2004) Behavioural responses to human disturbance: a matter of choice? Anim Behav 68:1065–1069
Béchet A, Giroux J-F, Gauthier G (2004) The effects of disturbance on behaviour, habitat use and energy of spring staging snow geese. J Appl Ecol 41:689–700
Brown C, Jones F, Braithwaite VA (2007) Correlation between boldness and body mass in natural populations of the poeciliid Brachyrhaphis episcope. J Fish Biol 71:1590–1601
Brown JS, Kotler BP (2004) Hazardous duty pay and the foraging cost of predation. Ecol Lett 7:999–1014
Buenestado FJ, Ferreras P, Blanco-Aguiar JA, Tortosa FS, Villafuerte R (2009) Survival and causes of mortality among wild Red-legged Partridges Alectoris rufa in southern Spain: implications for conservation. Ibis 151:720–730
Carrete M, Tella JL (2010) Individual consistency in flight initiation distances in burrowing owls: a new hypothesis on disturbance-induced habitat selection. Biol Lett. doi:10.1098/rsbl.2009.0739
Clark CW (1994) Antipredator behavior and the asset-protection principle. Behav Ecol 5:159–170
Coleman A, Richardson D, Schechter R, Blumstein DT (2008) Does habituation to humans influence predator discrimination in Gunther's dik-diks (Madoqua guentheri)? Biol Lett 4:250–252
Cooper WE Jr (2003) Shifted balance of risk and cost after autotomy affects use of cover, escape, activity and foraging in the keeled earless lizard (Holbrookia propinqua). Behav Ecol Sociobiol 54:179–187
Cooper WE Jr, Frederick WG (2007) Optimal flight initiation distance. J Theor Biol 244:59–67
Cooper WE Jr, Wilson DS (2008) How to stay alive after losing your tail. Behaviour 145:1085–1099
Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201
Davies M, Newsome D, Moncrieff D, Smith A (2007) Conserving the Black-flanked Rock-wallaby (Petrogale lateralis lateralis) through tourism: development of a habitat ranking system for translocated animals and the need for on-going management. Conserv Sci W Aust 6:1–12
Deecke VB, Slater PJB, Ford JKB (2002) Selective habituation shapes acoustic predator recognition in harbour seals. Nature 420:171–173
Díaz JA, Pérez-Tris J, Tellería JL, Carbonell R, Santos T (2005) Reproductive investment of a lacertid lizard in fragmented habitat. Conserv Biol 19:1578–1585
Dibattista JD, Feldheim KA, Gruber SH, Hendry AP (2007) When bigger is not better: selection against large size, high condition and fast growth in juvenile lemon sharks. J Evol Biol 20:201–212
Dobson FS, Michener GR (1995) Maternal traits and reproduction in Richardson's ground squirrels. Ecology 76:851–862
Domjan M (2003) The principles of learning and behavior. Belmont, California
Ellenberg U, Mattern T, Seddon PJ, Luna-Jorquera G (2006) Physiological and reproductive consequences of human disturbance in Humboldt penguins: the need for species specific visitor management. Biol Conserv 133:95–106
Ellenberg U, Mattern T, Seddon PJ (2009) Habituation potential of yellow-eyed penguins depends on sex, character and previous experience with humans. Anim Behav 77:289–296
Féret M, Gauthier G, Béchet A, Giroux J-F, Hobson KA (2003) Effect of a spring hunt on nutrient storage by greater snow geese in southern Quebec. J Wildl Manage 67:796–807
Fox AD, Madsen J (1997) Behavioural and distributional effects of hunting disturbance on waterbirds in Europe: implications for refuge design. J Appl Ecol 34:1–13
Fraser DF, Gilliam JF (1992) Nonlethal impacts of predator invasion: facultative suppression of growth and reproduction. Ecology 73:959–970
Frid A, Dill LM (2002) Human-caused disturbance stimuli as a form of predation risk. Conserv Ecol 6:11
Garner TWJ, Walker S, Bosch J, Leech S, Rowcliffe JM, Cunningham AA, Fisher MC (2009) Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118:783–791
Geist V (1975) On the management of mountain sheep: theoretical considerations (and discussion). In: Trefethen JB (ed) The wild sheep in modern North America. Boone & Crockett Club, Alexandrai, pp 77–105
Geist V (1978) Behavior. In: Schmidt JL, Gilbert DL (eds) Big game of North America: ecology and management. Stackpole Books, Harrisburg, pp 283–296
Gill JA, Norris K, Sutherland WJ (2001) Why behavioural responses may not reflect the population consequences of human disturbance. Biol Conserv 97:265–268
Hemmi JM (2005) Predator avoidance in fiddler crabs: 1. Escape decisions in relation to the risk of predation. Anim Behav 69:603–614
Hemmi JM, Merkle T (2009) High stimulus specificity characterizes anti-predator habituation under natural conditions. Proc R Soc B 276:4381–4388
Hjeljord O, Histøl T (1999) Range–body mass interactions of a northern ungulate—a test of a hypothesis. Oecologia 119:326–339
Hofman S, Henle K (2006) Male reproductive success and intrasexual selection in the common lizard determined by DNA-microsatellites. J Herpetol 40:1–6
Ikuta LA, Blumstein DT (2003) Do fences protect birds from human disturbance? Biol Conserv 112:447–452
Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67
Kloppers EL, St Claire CC, Hurd TE (2005) Predator-resembling aversive conditioning for managing habituated wildlife. Ecol Soc 10:31
Labra A, Leonard R (1999) Intraspecific variation in antipredator responses of three species of lizards (Liolaemus): possible effects of human presence. J Herpetol 33:441–448
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Lima SL, Bednekoff PE (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659
López P, Hawlena D, Polo V, Amo L, Martín J (2005) Sources of individual shy–bold variations in antipredator behaviour of male Iberian rock lizards. Anim Behav 69:1–9
Lord A, Waas JR, Innes J, Whittingham MJ (2001) Effects of human approaches to nests of northern New Zealand dotterels. Biol Conserv 98:233–240
Magle S, Zhu J, Crooks KR (2005) Behavioral responses to repeated human intrusion by black-tailed prairie dogs (Cynomis ludovicianus). J Mammal 86:524–530
Martín J, López P (1999) An experimental test of the costs of antipredatory refuge use in the wall lizard, Podarcis muralis. Oikos 84:499–505
Martínez-Abraín A, Oró D, Conesa D, Jiménez J (2008) Compromise between seabird enjoyment and disturbance: the role of observed and observers. Environ Conserv 35:104–108
Mccleery RA (2009) Changes in fox-squirrel anti-predators behaviors across the urban-rural gradient. Landscape Ecol 24:483–493
Müllner A, Linsenmair KE, Wikelski M (2004) Exposure to ecotourism reduces survival and affects stress response in hoatzin chicks (Opisthocomus hoazin). Biol Conserv 118:549–558
Naulleau G, Bonnet X (1996) Body condition threshold for breeding in a viviparous snake. Oecologia 107:1432–1939
Nisbet ICT (2000) Disturbance, habituation, and management of waterbirds colonies. Waterbirds 23:312–332
Olson TL, Gilbert BK, Squibb RC (1997) The effects of increasing human activity on brown bear use of an Alaskan river. Biol Conserv 82:95–99
Pauli JN, Buskirk SW (2007) Risk-disturbance overrides density dependence in a hunted colonial rodent, the black-tailed prairie dog Cynomys ludovicianus. J Appl Ecol 44:1219–1230
Peluc SI, Sillett TS, Rotenberry JT, Ghalambor CK (2008) Adaptive phenotypic plasticity in an island songbird exposed to a novel predation risk. Behav Ecol 19:830–835
Pérez-Tris J, Díaz JA, Tellería JL (2004) Loss of body mass under predation risk: cost of antipredatory behaviour or adaptive fit-for-escape. Anim Behav 67:511–521
Polo V, López P, Martín J (2010) Uncertainty about future predation risk modulates monitoring behaviour from refuges in lizards. Behav Ecol (in press)
Radder RS, Shanbhag BA (2004) Factors influencing offspring traits in the oviparous multi-clutched lizard, Calotes versicolor (Agamidae). J Biosci 29:105–110
Rankin CH et al (2009) Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiol Learn Mem 92:135–138
Reading CJ (2007) Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia 151:125–131
Réale D, Reader SM, Sol D, McDougall PT, Dingemanse N (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318
Rodriguez-Prieto I, Fernández-Juricic E, Martín J, Regis Y (2009) Antipredator behavior in blackbirds: habituation complements risk allocation. Behav Ecol 20:371–377
Runyan AM, Blumstein DT (2004) Do individual differences influence flight initiation distance? J Wildl Manage 68:1124–1129
Salvador A, Martín J, López P (1995) Tail loss reduces home range size and access to females in male lizards, Psammodromus algirus. Behav Ecol 6:382–387
Salvador A, Díaz JA, Veiga JP, BloorP BRP (2008) Correlates of reproductive success in male lizards of the alpine species Iberolacerta cyreni. Behav Ecol 19:169–176
Sapolsky RM (1992) Neuroendocrinology of the stress response. In: Becker JB, Breedlove SM, Crews D (eds) Behavioral Endocrinology. Massachusetts Institute of Technnology Press, Cambridge, pp 287–324
Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163
Sheriff MJ, Krebs CJ, Boonstra R (2009) The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J Anim Ecol 78:1249–1258
Shine R, LeMaster LP, Moore IT, Olsson MM, Mason RT (2001) Bumpus in the snake den: effects of sex, size, and body condition on mortality of red-sided garter snakes. Evolution 55:598–604
Sinervo B, Doughty P, Huey RB, Zamudio K (1992) Allometric engineering: a causal analysis of natural selection on offspring size. Science 258:1927–1930
Smith BR, Blumstein DT (2008) Fitness consequences of personality: a meta-analysis. Behav Ecol 19:448–455
Stolen ED (2003) The effects of vehicle passage on foraging behavior of wading birds. Waterbirds 26:429–436
Sutherlan WJ (2007) Future directions in disturbance reearch. Ibis 149:120–124
Tarlow E, Blumstein DT (2007) Evaluating methods to quantify anthropogenic stressors on wild animals. Appl Anim Behav Sci 102:429–451
Taylor AR, Knight RL (2003) Wildlife responses to recreation and associated visitor perceptions. Ecol Appl 13:951–963
Taylor SS, Jamieson IG (2007) Factors affecting the survival of founding individuals in translocated New Zealand Saddlebacks Philesturnus carunculatus. Ibis 149:783–791
Thompson MJ, Henderson RE (1998) Elk habituation as a credibility challenge for wildlife professionals. Wildl Soc Bull 26:477–483
Van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142
Walker BG, Boersma PD, Wingfield JC (2006) Habituation of adult magellanic penguins to human visitation as expressed trough behavior and corticosterone secretion. Conserv Biol 20:146–154
Ward AJW, Thomas P, Hart PJB, Krause J (2004) Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol 55:561–568
Wauters LA, Dhondt AA (1995) Lifetime reproductive success and its correlates in female Eurasian red squirrels. Oikos 72:402–410
Whittingham MJ, Stephens PA, Bradbury RB, Freckleton RP (2006) Why do we still use stepwise modelling in ecology and behaviour? J Anim Ecol 75:1182–1189
Wilson ADM, Godin JGJ (2009) Boldness and behavioral syndromes in the bluegill sunfish, Lepomis macrochirus. Behav Ecol 20:231–237
Ydenberg RC, Dill LM (1986) The economics of fleeing from predators. Adv Study Behav 16:229–249
Acknowledgements
We thank “El Ventorrillo” MNCN Field Station for the use of their facilities. Financial funding was provided by the project MCI-CGL 2008-02119. IRP was supported by a postgraduate grant from the Spanish National Research Council (CSIC).
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Rodríguez-Prieto, I., Martín, J. & Fernández-Juricic, E. Habituation to low-risk predators improves body condition in lizards. Behav Ecol Sociobiol 64, 1937–1945 (2010). https://doi.org/10.1007/s00265-010-1004-2
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DOI: https://doi.org/10.1007/s00265-010-1004-2