Individual variation in behavioural plasticity: Direct and indirect effects of boldness, exploration and sociability on habituation to predators in lizards

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1703, 2011, Pages 266-273

  Rodríguez Prieto, Iñaki ^a   Martín, José ^a   Fernández Juricic, Esteban ^b  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^b PURDUE UNIVERSITY   (United States)

Author keywords

Behavioural plasticity; Boldness; Exploration; Habituation; Personality; Sociability

Indexed keywords

BEHAVIORAL RESPONSE; CONSPECIFIC; HABITUATION; LIZARD; PHENOTYPIC PLASTICITY; RISK ASSESSMENT; SOCIAL BEHAVIOR;

PODARCIS; SQUAMATA;

EID: 78650440224     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.1194     Document Type: Conference Paper

References (61)

1. Bell, A. M., Hankison, S. J. & Laskowski, K. L. 2009 The repeatability of behaviour: a meta-analysis. Anim. Behav. 11, 771-783. (doi:10.1016/j.anbehav. 2008.12.022)
2. Dall, S. R. X., Houston, A. I. & McNamara, J. M. 2004 The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol. Lett. 7, 734-739. (doi:10.1111/j.1461-0248.2004.00618.x) (Pubitemid 39040218)
3. Réale, D., Reader, S. M., Sol, D., McDougall, R T. & Dingemanse, N. 2007 Integrating animal temperament within ecology and evolution. Biol. Rev. 82, 291-318. (doi:10.1111/j.l469-185X.2007.00010.x)
4. Sih, A., Bell, A. & Johnson, J. C. 2004 Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol. Evol. 19, 372-378. (doi:10.1016/j.tree.2004.04.009) (Pubitemid 38800923)
5. Dingemanse, N. J., Both, C, Drent, R J., Van Oers, K. & Van Noordwijk, A. J. 2002 Repeatability and heritability of exploratory behaviour in great tits from the wild. Anim. Behav. 64, 929-937. (doi:10.1006/anbe.2002. 2006) (Pubitemid 36784817)
6. Drent, R J., Van Oers, K. & Van Noordwijk, A. J. 2003 Realized heritability of personalities in the great tit (Parus major). Proc. R. Soc. Lond. B 270, 45-51. (doi:10.1098/rspb.2002.2168) (Pubitemid 36140421)
7. Van Oers, K., de Jong, G., Van Noordwijk, A. J., Kempenaers, B. & Drent, R J. 2005 Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour 142, 1185-1206. (doi: 10.1163/ 156853905774539364) (Pubitemid 44430956)
8. Dingemanse, N. J. & Réale, D. 2005 Natural selection and animal personality. Behaviour 142, 1159-1184. (doi:10.1163/156853905774539445) (Pubitemid 44430955)
9. Smith, B. R. & Blumstein, D. T. 2008 Fitness consequences of personality: a meta-analysis. Behav. Ecol. 19, 448-455. (doi:10.1093/beheco/ arml44)
10. Dingemanse, N. J., Kazem, A. J. M., Réale, D. & Wright, J. 2010 Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol. Evol. 25, 81-89. (doi:10.1016/j.tree.2009.07.013)
11. Biro, R A., Beckmann, C. & Stamps, J. A. 2010 Small within-day increases in temperature affects boldness and alters personality in coral reef fish. Proc. R. Soc. B 277, 71-77. (doi:10.1098/rspb.2009.1346)
12. Bell, A. M. & Sih, A. 2007 Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol. Lett. 10, 828-834. (doi: 10.1111/j.1461-0248.2007.01081.x) (Pubitemid 47174413)
13. Briffa, M., Rundle, S. D. & Fryer, A. 2008 Comparing the strength of behavioural plasticity and consistency across situations: animal personalities in the hermit crab Pagurus bernhardus. Proc. R. Soc. B 275, 1305-1311. (doi: 10.1098/rspb.2008.0025) (Pubitemid 351581484)
14. Nussey, D. H., Wilson, A. J. & Brommer, J. E. 2007 The evolutionary ecology of individual phenotypic plasticity in wild populations. J. Evol. Biol. 20, 831-844. (doi: 10.1111/j.1420-9101.2007.01300.x) (Pubitemid 46663106)
15. Hemmi, J. & Merkle, T. 2009 High stimulus specificity characterizes anti-predator habituation under natural conditions. Proc. R. Soc. B 276, 4381-4388. (doi:10.1098/rspb.2009.1452)
16. Shettleworth, S. J. 2010 Cognition, evolution and behavior, 2nd ed. Oxford, UK: Oxford University Press.
17. Ellenberg, U, Mattern, T. & Seddon, P. J. 2009 Habituation potential of yellow-eyed penguins depends on sex, character and previous experience with humans. Anim. Behav. 77, 289-296. (doi:10.1016/j.anbehav.2008.09.021)
18. Rodriguez-Prieto, I., Fernández-Juricic, E., Martín, J. & Regis, Y. 2009 Antipredator behavior in blackbirds: habituation complements risk allocation. Behav. Ecol. 20, 371-377. (doi:10.1093/beheco/ arnl51)
19. Stolen, E. D. 2003 The effects of vehicle passage on foraging behavior of wading birds. Waterbirds 26, 429-436. (doi:10.1675/1524-4695(2003)026[0429:TE OVPO]2.0.CO;2)
20. Runyan, A. M. & Blumstein, D. T. 2004 Do individual differences influence flight initiation distance? J. Wildl. Mngmt. 68, 1124-1129. (doi:10.2193/0022-541X(2004)068[1124:DIDIFI]2.0.CO;2) (Pubitemid 40107319)
21. Martin, J. G. A. & Réale, D. 2008 Temperament, risk assessment and habituation to novelty in eastern chipmunks, Tamias striatus. Anim. Behav. 75, 309-318. (doi:10.1016/j.anbehav.2007.05.026) (Pubitemid 350298105)
22. Rodríguez-Prieto, I., Martín, J. & Fernández- Juricic, E. In press. Habituation to low-risk predators improves body condition in lizards. Behav. Ecol. Sociobiol.
23. Koolhaas, J. M., Korte, S. M., De Boer, S. F, Van Der Vegt, B. J., Van Reenen, C. G., Hopster, H., De Jong, I. C, Ruis, M. A. W. & Blokhuis, H. J. 1999 Coping styles in animals: current status in behavior and stress-physiology. Neurosci. Biobehav. R 23, 925-935. (doi:10.1016/S0149-7634(99)00026-3) (Pubitemid 29502398)
24. Jensen, P. 2002 The ethology of domestic animals: an introductory text. CABI Publishing.
25. Carere, C, Drent, P. J., Koolhaas, J. M. & Groothuis, T. G. G. 2004 Personalities in great tits, Parus major, stability and consistency. Anim. Behav. 70, 795-805. (doi:10.1016/j.anbehav.2005.01.003)
26. Crusio, W. E. 2001 Genetic dissection of mouse exploratory behaviour. Behav. Brain Res. 125, 127-132. (doi:10.1016/S0166-4328(01)00280-7) (Pubitemid 33000450)
27. Greenberg, R. & Mettke-Hoffmann, C. 2001 Ecological aspects of neophobia and exploration. Curr. Ornithol. 16, 119-178.
28. Tebbich, S., Fessl, B. & Blomqvist, D. 2009 Exploration and ecology in Darwin's finches. Evol. Ecol. 23, 591-605. (doi:10.1007/s10682-008-9257-1)
29. Cote, J., Dreiss, A. & Clobert, J. 2008 Social personality trait and fitness. Proc. R. Soc. B 275, 2851-2858. (doi:10.1098/rspb.2008.0783) (Pubitemid 352790139)
30. Desforges, M. F. & Wood-Gush, D. G. M. 1975 A behavioural comparison of domestic and mallard ducks. Habituation and flight reaction. Anim. Behav. 23, 692-697. (doi:10.1016/0003-3472(75)90145-1)
31. López, P., Hawlena, D., Polo, V., Amo, L. & Martín, J. 2005 Sources of individual shy-bold variations in antipredator behaviour of male Iberian wall lizards. Anim. Behav. 69, 1-9. (doi:10.1016/j.anbehav.2004.05.010) (Pubitemid 40033305)
32. Cote, J. & Clobert, J. 2007 Social personalities influence natal dispersal in a lizard. Proc. R. Soc. B 274, 383-390. (doi:10.1098/rspb.2006. 3734) (Pubitemid 47055462)
33. Aragón, P., López, P. & Martín, J. 2001 Seasonal changes in activity and spatial and social relationships of the Iberian rock-lizard Lacerta monticola. Can. J. Zool. 79, 1965-1971. (doi:10.1139/cjz-79- 11-1965) (Pubitemid 34190608)
34. Kerr, G. D. & Bull, C. M. 2006 Movement patterns in the monogamous sleepy lizard (Tiliqua rugosa): effects of gender, drought, time of year and time of day. J. Zool. 269, 137-147.
35. Avery, R. A. 1993 Experimental analysis of lizard pause-travel movement: pauses increase probability of prey capture. Amphibia-Reptilia 14, 423-427. (doi: 10.1163/156853893X00110)
36. Van Damme, R., Aerts, P. & Vanhooydonck, B. 1997 No trade-off between sprinting and climbing in two populations of the lizard Podarcis hispanica (Reptilia: Lacertidae). Biol. J. Linn. Soc. 60, 493-503. (doi: 10.1006/bijl.l996.0115)
37. Galán, P. 2003 Reproductive characteristics of an insular population of the lizard Podarcis hispanica from Northwest Spain (Cíes Islands, Galicia). Copeia 2003, 657-665. (doi: 10.1643/CH-02-235R1)
38. Barbadillo, L. J., Lacomba, J. I., Pérez-Mellado, V, Sancho, V. & López-Jurado, L. F. 1999 Anfibios y reptiles de la Península Ibérica. Barcelona, Spain: Planeta.
39. Rankin, C. H. et al. 2009 Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiol. Learn. Mem. 92, 135-138. (doi:10.1016/j.nlm.2008.09.012)
40. Hemmi, J. M. 2005 Predator avoidance in fiddler crabs. 1. Escape decisions in relation to the risk of predation. Anim. Behav. 69, 603-614. (doi:10.1016/j.anbehav.2004.06.018) (Pubitemid 40253026)
41. Lord, A., Waas, J. R., Innes, J. & Whittingham, M. J. 2001 Effects of human approaches to nests of northern New Zealand dotterels. Biol. Conserv. 98, 233-240. (doi: 10.1016/S0006-3207(00)00158-0) (Pubitemid 32228367)
42. Magle, S., Zhu, J. & Crooks, K. R. 2005 Behavioral responses to repeated human intrusion by black-tailed prairie dogs (Cynomis ludovicianus). J. Mammal. 86, 524-530. (doi:10.1644/1545-1542(2005)86[524:BRT RHI]2.0.CO;2)
43. Walker, B. G, Boersma, P. D. & Wingfield, J. C. 2006 Habituation of adult magellanic penguins to human visitation as expressed trough behavior and corticosterone secretion. Conserv. Biol. 20, 146-154. (doi:10.1111/j.1523-1739. 2005.00271.x)
44. MacKinnon, D. P., Fairchild, A. J. & Fritz, M. S. 2007 Mediation analysis. Ann. Rev. Psychol. 58, 593-614. (doi:10.1146/annurev.psych.58.110405. 085542)
45. Sih, A., Lauer, M. & Krupa, J. J. 2002 Path analysis and the relative importance of male-female conflict, female choice and male-male competition in water striders. Anim. Behav. 63, 1079-1089. (doi:10.1006/anbe.2002.2002) (Pubitemid 34995886)
46. Bentler, P. M. 1989 EQS structural equations program manual. Los Angeles, CA: BMDP Statistical Software.
47. Iriondo, J. M., Albert, M. J. & Escudero, A. 2003 Structural equation modelling: an alternative for assessing causal relationships in threatened plant populations. Biol. Conserv 113, 367-377. (doi:10.1016/S0006-3207(03)00129- 0) (Pubitemid 36990606)
48. Pedhazur, E. J. 1982 Multiple regression in behavioural research. Explanation and prediction. New York, NY: Holt, Rinehart & Winston.
49. Burnham, K. P. & Anderson, D. R. 2002 Model selection and multimodel inference: a practical information theoretic approach. New York, NY: Springer.
50. Kenny, D. A., Kashy, D. A. & Bolger, N. 1998 Data analysis in social psychology. In The handbook of social psychology, vol. 1 (eds D. Gilbert, S. Fiske & G. Lindzey), pp. 233-265, 4th edn. Boston, MA: McGraw-Hill.
51. Bollen, K. A. 1989 Structural equations with latent variables. New York, NY: John Wiley & Sons
52. ASAB/ABS 2006 Guidelines for the treatment of animals in behavioural research and teaching. Anim. Behav. 71, 245-253. (doi:10.1016/j.anbehav.2005.10. 001)
53. ASIH 2004 Guidelines for use of live amphibians and reptiles in field and laboratory research, 2nd edn. Lawrence, KA: Herpetological Animal Care and Use Committee (HACC) of the American Society of Ichthyologists and Herpetologists.
54. Guillette, L. M., Reddon, A. R., Hurd, P. L. & Sturdy, C. B. 2009 Exploration of a novel space is associated with individual differences in learning speed in black- capped chickadees, Poecile atricapillus. Behav. Process. 82, 265-270. (doi:10.1016/j.beproc.2009.07.005)
55. Dingemanse, N. J., Both, C, Van Noordwijk, A. J., Rutten, A. L. & Drent, P. J. 2003 Natal dispersal and personalities in great tits (Parus major). Proc. R. Soc. Lond. B 270, 741-747. (doi:10.1098/rspb.2002.2300) (Pubitemid 36433927)
56. Cote, J., Fogarty, S., Weinersmith, K, Brodin, T. & Sih, A. 2010 Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). Proc. R. Soc. B 277, 1571-1579. (doi:10.1098/rspb.2009.2128)
57. Duckworth, R. A. & Badyaev, A. V. 2007 Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proc. Natl Acad. Sci. USA 104, 15017-15022. (doi:10.1073/pnas.0706174104) (Pubitemid 47619585)
58. Creel, S. & Christianson, D. 2008 Relationships between direct predation and risk effects. Trends Ecol. Evol. 23, 194-201.
59. Verbeek, M. E. M., Drent, P. J. & Wiepkema, P. R. 1994 Consistent individual differences in early exploratory behaviour of male great tits. Anim. Behav. 48, 1113-1121. (doi: 10.1006/anbe.1994.1344)
60. Auld, J. R., Agrawal, A. A. & Relyea, R. A. 2010 Reevaluating the costs and limits of adaptive phenotypic plasticity. Proc. R. Soc. B 277, 503-511. (doi:10.1098/rspb.2009.1355)
61. Dall, S. R. X., Giraldeau, L.-A., Olsson, O., McNamara, J. M. & Stephens, D. W. 2005 Information and its use by animals in evolutionary ecology. Trends Ecol. Evol. 20, 187-193. (doi:10.1016/j.tree.2005.01.010) (Pubitemid 40359265)