Demystifying animal 'personality' (or not): Why individual variation matters to experimental biologists

Journal of Experimental Biology

Volumn 219, Issue 24, 2016, Pages 3832-3843

  Roche, Dominique G ^a   Careau, Vincent ^b   Binning, Sandra A ^a  

^a UNIVERSITY OF NEUCHÂTEL   (Switzerland)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Behaviour; Phenotypic variation; Physiology; Reaction norm; Repeatability; Temperament

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; BIOLOGY; PERSONALITY; PHENOTYPE; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGY; PERSONALITY; PHENOTYPE;

EID: 85006380270     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.146712     Document Type: Review

References (147)

1. Adolph, S. C. and Pickering, T. (2008). Estimating maximum performance: effects of intraindividual variation. J. Exp. Biol. 211, 1336-1343.
2. Adriaenssens, B. and Johnsson, J. I. (2013). Natural selection, plasticity and the emergence of a behavioural syndrome in the wild. Ecol. Lett. 16, 47-55.
3. Ariyomo, T. O. and Watt, P. J. (2012). The effect of variation in boldness and aggressiveness on the reproductive success of zebrafish. Anim. Behav. 83, 41-46.
4. Arnold, S. J. and Bennett, A. F. (1984). Behavioural variation in natural populations. III. Antipredator displays in the garter snake Thamnophis radix. Anim. Behav. 32, 1108-1118.
5. Auer, S. K., Bassar, R. D., Salin, K. and Metcalfe, N. B. (2016). Repeatability of metabolic rate is lower for animals living under field versus laboratory conditions. J. Exp. Biol. 219, 631-634.
6. Balzarini, V., Taborsky, M., Wanner, S., Koch, F. and Frommen, J. G. (2014). Mirror, mirror on the wall: the predictive value of mirror tests for measuring aggression in fish. Behav. Ecol. Sociobiol. 68, 871-878.
7. Barber, I. and Dingemanse, N. J. (2010). Parasitism and the evolutionary ecology of animal personality. Philos. Trans. R. Soc. B Biol. Sci. 365, 4077-4088.
8. Beckmann, C. and Biro, P. A. (2013). On the validity of a single (boldness) assay in personality research. Ethology 119, 937-947.
9. Bennett, A. F. (1980). The thermal dependence of lizard behaviour. Anim. Behav. 28, 752-762.
10. Bennett, A. F. (1987). Interindividual variability: an underutilized resource. In New Directions in Ecological Physiology (ed. M. Feder, A. Bennett, W. Burggren and R. Huey), pp. 147-169. Cambridge: Cambridge University Press.
11. Binning, S. A., Barnes, J. I., Davies, J. N., Backwell, P. R. Y., Keogh, J. S. and Roche, D. G. (2014). Ectoparasites modify escape behaviour, but not performance, in a coral reef fish. Anim. Behav. 93, 1-7.
12. Biro, P. A. (2012). Do rapid assays predict repeatability in labile (behavioural) traits? Anim. Behav. 83, 1295-1300.
13. Biro, P. A. and Dingemanse, N. J. (2009). Sampling bias resulting from animal personality. Trends Ecol. Evol. 24, 66-67.
14. Biro, P. A. and Stamps, J. A. (2008). Are animal personality traits linked to lifehistory productivity? Trends Ecol. Evol. 23, 361-368.
15. Biro, P. A. and Stamps, J. A. (2010). Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol. Evol. 25, 653-659.
16. Biro, P. A. and Stamps, J. A. (2015). Using repeatability to study physiological and behavioural traits: ignore time-related change at your peril. Anim. Behav. 105, 223-230.
17. Blumstein, D. T. (2003). Flight-initiation distance in birds is dependent on intruder starting distance. J. Wildl. Manage. 67, 852-857.
18. Boake, C. R. B. (1989). Repeatability: its role in evolutionary studies of mating behavior. Evol. Ecol. 3, 173-182.
19. Boake, C. R. B., Arnold, S. J., Breden, F., Meffert, L. M., Ritchie, M. G., Taylor, B. J., Wolf, J. B. and Moore, A. J. (2002). Genetic tools for studying adaptation and the evolution of behavior. Am. Nat. 160, S143-S159.
20. Bolnick, D. I., Svanbäck, R., Fordyce, J. A., Yang, L. H., Davis, J. M., Hulsey, C. D. and Forister, M. L. (2003). The ecology of individuals: incidence and implications of individual specialization. Am. Nat. 161, 1-28.
21. Boon, A. K., Réale, D. and Boutin, S. (2008). Personality, habitat use, and their consequences for survival in North American red squirrels Tamiasciurus hudsonicus. Oikos 117, 1321-1328.
22. Both, C., Dingemanse, N. J., Drent, P. J. and Tinbergen, J. M. (2005). Pairs of extreme avian personalities have highest reproductive success. J. Anim. Ecol. 74, 667-674.
23. Boyer, N., Réale, D., Marmet, J., Pisanu, B. and Chapuis, J.-L. (2010). Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. J. Anim. Ecol. 79, 538-547.
24. Brommer, J. E. (2013). On between-individual and residual (co)variances in the study of animal personality: are you willing to take the "individual gambit"? Behav. Ecol. Sociobiol. 67, 1027-1032.
25. Browman, H. I. (2016). Applying organized scepticism to ocean acidification research. ICES J. Mar. Sci. 73, 529-536.
26. Burns, J. G. (2008). The validity of three tests of temperament in guppies (Poecilia reticulata). J. Comp. Psychol. 122, 344-356.
27. Byrnes, E. E. and Brown, C. (2016). Individual personality differences in Port Jackson sharks Heterodontus portusjacksoni. J. Fish Biol. 89, 1142-1157.
28. Careau, V. and Garland, T. (2012). Performance, personality, and energetics: correlation, causation, and mechanism. Physiol. Biochem. Zool. 85, 543-571.
29. Careau, V., Thomas, D., Humphries, M. M. and Réale, D. (2008). Energy metabolism and animal personality. Oikos 117, 641-653.
30. Careau, V., Montiglio, P.-O., Garant, D., Pelletier, F., Speakman, J. R., Humphries, M. M. and Réale, D. (2015). Energy expenditure and personality in wild chipmunks. Behav. Ecol. Sociobiol. 69, 653-661.
31. Carere, C. and van Oers, K. (2004). Shy and bold great tits (Parus major): body temperature and breath rate in response to handling stress. Physiol. Behav. 82, 905-912.
32. Carter, A. J., Heinsohn, R., Goldizen, A. W. and Biro, P. A. (2012). Boldness, trappability and sampling bias in wild lizards. Anim. Behav. 83, 1051-1058.
33. Carter, A. J., Feeney, W. E., Marshall, H. H., Cowlishaw, G. and Heinsohn, R. (2013). Animal personality: what are behavioural ecologists measuring? Biol. Rev. 88, 465-475.
34. Chabot, D., Steffensen, J. F. and Farrell, A. P. (2016). The determination of standard metabolic rate in fishes. J. Fish Biol. 88, 81-121.
35. Chown, S. L. (2001). Physiological variation in insects: hierarchical levels and implications. J. Insect Physiol. 47, 649-660.
36. Clark, A. B. and Ehlinger, T. J. (1987). Pattern and adaptation in individual behavioral differences. In Perspectives in Ethology (ed. P. P. G. Bateson and P. H. Klopfer), pp. 1-47. Boston, MA: Springer.
37. Cleasby, I. R., Nakagawa, S. and Schielzeth, H. (2015). Quantifying the predictability of behaviour: statistical approaches for the study of betweenindividual variation in the within-individual variance. Methods Ecol. Evol. 6, 27-37.
38. Cockrem, J. F. (2007). Stress, corticosterone responses and avian personalities. J. Ornithol. 148, 169-178.
39. Cole, E. F. and Quinn, J. L. (2012). Personality and problem-solving performance explain competitive ability in the wild. Proc. R. Soc. B Biol. Sci. 279, 1168-1175.
40. Conrad, J. L., Weinersmith, K. L., Brodin, T., Saltz, J. B. and Sih, A. (2011). Behavioural syndromes in fishes: a review with implications for ecology and fisheries management. J. Fish Biol. 78, 395-435.
41. Conradsen, C., Walker, J. A., Perna, C. and McGuigan, K. (2016). Repeatability of locomotor performance and morphology-locomotor performance relationships. J. Exp. Biol. 219, 2888-2897.
42. Costantini, D., Carere, C., Caramaschi, D. and Koolhaas, J. M. (2008). Aggressive and non-aggressive personalities differ in oxidative status in selected lines of mice (Mus musculus). Biol. Lett. 4, 119-122.
43. Cote, J., Clobert, J., Brodin, T., Fogarty, S. and Sih, A. (2010). Personalitydependent dispersal: characterization, ontogeny and consequences for spatially structured populations. Philos. Trans. R. Soc. B Biol. Sci. 365, 4065-4076.
44. Crawford, D. L. and Oleksiak, M. F. (2007). The biological importance of measuring individual variation. J. Exp. Biol. 210, 1613-1621.
45. Dall, S. R. X. and Griffith, S. C. (2014). An empiricist guide to animal personality variation in ecology and evolution. Front. Ecol. Evol. 2, 3.
46. Dammhahn, M. (2012). Are personality differences in a small iteroparous mammal maintained by a life-history trade-off? Proc. R. Soc. B Biol. Sci. 279, 2645-2651.
47. Dammhahn, M. and Almeling, L. (2012). Is risk taking during foraging a personality trait? A field test for cross-context consistency in boldness. Anim. Behav. 84, 1131-1139.
48. Darveau, C.-A., Billardon, F. and Bélanger, K. (2014). Intraspecific variation in flight metabolic rate in the bumblebee Bombus impatiens: repeatability and functional determinants in workers and drones. J. Exp. Biol. 217, 536-544.
49. David, M. and Dall, S. R. X. (2016). Unravelling the philosophies underlying 'animal personality' studies: a brief re-appraisal of the field. Ethology 122, 1-9.
50. David, M., Auclair, Y. and Cézilly, F. (2011). Personality predicts social dominance in female zebra finches, Taeniopygia guttata, in a feeding context. Anim. Behav. 81, 219-224.
51. Diaz Pauli, B., Wiech, M., Heino, M. and Utne-Palm, A. C. (2015). Opposite selection on behavioural types by active and passive fishing gears in a simulated guppy Poecilia reticulata fishery. J. Fish Biol. 86, 1030-1045.
52. Dingemanse, N. J. and Araya-Ajoy, Y. G. (2015). Interacting personalities: behavioural ecology meets quantitative genetics. Trends Ecol. Evol. 30, 88-97.
53. Dingemanse, N. J. and Dochtermann, N. A. (2013). Quantifying individual variation in behaviour: mixed-effect modelling approaches. J. Anim. Ecol. 82, 39-54.
54. Dingemanse, N. J. and Réale, D. (2005). Natural selection and animal personality. Behaviour 142, 1159-1184.
55. Dingemanse, N. J., Kazem, A. J. N., Réale, D. and Wright, J. (2010). Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol. Evol. 25, 81-89.
56. Dingemanse, N. J., Bouwman, K. M., van del Pol, M., van Overveld, T., Patrick, S. C., Matthysen, E. and Quinn, J. L. (2012). Variation in personality and behavioural plasticity across four populations of the great tit Parus major. J. Anim. Ecol. 81, 116-126.
57. DiRienzo, N. and Montiglio, P.-O. (2015). Four ways in which data-free papers on animal personality fail to be impactful. Front. Ecol. Evol. 3, 23.
58. Dohm, M. R. D. (2002). Repeatability estimates do not always set an upper limit to heritability. Funct. Ecol. 16, 273-280.
59. Dohm, M. R., Hayes, J. P. and Garland, T., Jr. (2001). The quantitative genetics of maximal and basal rates of oxygen consumption in mice. Genetics 159, 267-277.
60. Domenici, P., Lefrancois, C. and Shingles, A. (2007). Hypoxia and the antipredator behaviours of fishes. Philos. Trans. R. Soc. B Biol. Sci. 362, 2105-2121.
61. Domenici, P., Herbert, N. A., Lefrançois, C., Steffensen, J. F. and McKenzie, D. J. (2013). The effect of hypoxia on fish swimming performance and behaviour. In Swimming Physiology of Fish: Towards Using Exercise to Farm a Fit Fish in Sustainable Aquaculture (ed. P. A. Palstra and V. J. Planas), pp. 129-159. Berlin; Heidelberg: Springer Berlin Heidelberg.
62. Falconer, D. S. and Mackay, T. F. C. (1996). Introduction to Quantitative Genetics. Essex, UK: Longman.
63. Farrell, W. J. and Wilczynski, W. (2006). Aggressive experience alters place preference in green anole lizards, Anolis carolinensis. Anim. Behav. 71, 1155-1164.
64. Freeman, H. D. and Gosling, S. D. (2010). Personality in nonhuman primates: a review and evaluation of past research. Am. J. Primatol. 72, 653-671.
65. Garamszegi, L. Z., Eens, M. and Török, J. (2009). Behavioural syndromes and trappability in free-living collared flycatchers, Ficedula albicollis. Anim. Behav. 77, 803-812.
66. Garland, T. (1988). Genetic basis of activity metabolism. I. Inheritance of speed, stamina, and antipredator displays in the garter snake Thamnophis sirtalis. Evolution 42, 335-350.
67. Garland, T. (1994). Quantitative genetics of locomotor behavior and physiology in a garter snake. In Quantitative Genetic Studies of Behavioral Evolution (ed. C. R. B. Boake), pp. 251-276. Chicago: University of Chicago Press.
68. Gosling, S. D. (2001). From mice to men: what can we learn about personality from animal research? Psychol. Bull. 127, 45-86.
69. Gosling, S. D. (2008). Personality in non-human animals. Soc. Personal. Psychol. Compass 2, 985-1001.
70. Gould, S. J. (1985). The median isn't the message. Discover 6, 40-42.
71. Griffin, A. S., Guillette, L. M. and Healy, S. D. (2015). Cognition and personality: an analysis of an emerging field. Trends Ecol. Evol. 30, 207-214.
72. Hadfield, J. D. (2010). MCMC methods for multi-response generalised linear mixed models: The MCMCglmm R package. J. Stat. Soft. 33, 1-22.
73. A receptor functioning. Proc. R. Soc. B Biol. Sci. 281, 20132509.
74. Harris, S., Ramnarine, I. W., Smith, H. G. and Pettersson, L. B. (2010). Picking personalities apart: estimating the influence of predation, sex and body size on boldness in the guppy Poecilia reticulata. Oikos 119, 1711-1718.
75. Hayes, J. P. and Jenkins, S. H. (1997). Individual variation in mammals. J. Mammal. 78, 274-293.
76. Hayes, J. P., Speakman, J. R. and Racey, P. A. (1992). Sampling bias in respirometry. Physiol. Zool. 65, 604-619.
77. Henderson, C. R. (1982). Analysis of covariance in the mixed model: higher-level, nonhomogeneous, and random regressions. Biometrics 38, 623-640.
78. Herborn, K. A., Macleod, R., Miles, W. T. S., Schofield, A. N. B., Alexander, L. and Arnold, K. E. (2010). Personality in captivity reflects personality in the wild. Anim. Behav. 79, 835-843.
79. Houle, D. (1991). Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters. Evolution 45, 630-648.
80. Huntingford, F. A. (1976). The relationship between anti-predator behaviour and aggression among conspecifics in the three-spined stickleback, Gasterosteus aculeatus. Anim. Behav. 24, 245-260.
81. Jolles, J. W., Fleetwood-Wilson, A., Nakayama, S., Stumpe, M. C., Johnstone, R. A. and Manica, A. (2015). The role of social attraction and its link with boldness in the collective movements of three-spined sticklebacks. Anim. Behav. 99, 147-153.
82. Jornod, M. and Roche, D.G. (2015). Inter-vs intra-individual variation and temporal repeatability of escape responses in the coral reef fish Amblyglyphidodon curacao. Biol. Open 4, 1395-1399.
83. Killen, S. S., Marras, S., Metcalfe, N. B., McKenzie, D. J. and Domenici, P. (2013). Environmental stressors alter relationships between physiology and behaviour. Trends Ecol. Evol. 28, 651-658.
84. Killen, S. S., Nati, J. J. H. and Suski, C. D. (2015). Vulnerability of individual fish to capture by trawling is influenced by capacity for anaerobic metabolism. Proc. R. Soc. B Biol. Sci. 282, 20150603.
85. Killen, S. S., Adriaenssens, B., Marras, S., Claireaux, G. and Cooke, S. J. (2016). Context dependency of trait repeatability and its relevance for management and conservation of fish populations. Conserv. Physiol. 4, cow007.
86. Kolok, A. S. (1999). Interindividual variation in the prolonged locomotor performance of ectothermic vertebrates: a comparison of fish and herpetofaunal methodologies and a brief review of the recent fish literature. Can. J. Fish. Aquat. Sci. 56, 700-710.
87. 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. and Blokhuis, H. J. (1999). Coping styles in animals: current status in behavior and stress-physiology. Neurosci. Biobehav. Rev. 23, 925-935.
88. Koski, S. E. (2014). Broader horizons for animal personality research. Front. Ecol. Evol. 2, 70.
89. Koski, S. E. and Burkart, J. M. (2015). Common marmosets show social plasticity and group-level similarity in personality. Sci. Rep. 5, 8878.
90. Kurvers, R. H. J. M., Eijkelenkamp, B., van Oers, K., van Lith, B., van Wieren, S. E., Ydenberg, R. C. and Prins, H. H. T. (2009). Personality differences explain leadership in barnacle geese. Anim. Behav. 78, 447-453.
91. Kurvers, R. H. J. M., Van Oers, K., Nolet, B. A., Jonker, R. M., Van Wieren, S. E., Prins, H. H. T. and Ydenberg, R. C. (2010). Personality predicts the use of social information. Ecol. Lett. 13, 829-837.
92. Lacy, R. C., Alaks, G. and Walsh, A. (2013). Evolution of Peromyscus leucopus mice in response to a captive environment. PLoS ONE 8, e72452.
93. Laming, S. R., Jenkins, S. R. and McCarthy, I. D. (2013). Repeatability of escape response performance in the queen scallop, Aequipecten opercularis. J. Exp. Biol. 216, 3264-3272.
94. Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. and Getz, W. M. (2005). Superspreading and the effect of individual variation on disease emergence. Nature 438, 355-359.
95. Lopes, P. C. (2016). Why are behavioral and immune traits linked? Horm. Behav. http://dx.doi.org/10.1016/j.yhbeh.2016.09.008.
96. Lopes, P. C., Adelman, J., Wingfield, J. C. and Bentley, G. E. (2012). Social context modulates sickness behavior. Behav. Ecol. Sociobiol. 66, 1421-1428.
97. Losos, J. B., Creer, D. A. and Schulte, J. A. II (2002). Cautionary comments on the measurement of maximum locomotor capabilities. J. Zool. 258, 57-61.
98. Lynch, M. and Walsh, J. B. (1998). Genetics and Analysis of Quantitative traits. Sunderland, Massachusetts: Sinauer Associates.
99. MacKenzie, S., Ribas, L., Pilarczyk, M., Capdevila, D. M., Kadri, S. and Huntingford, F. A. (2009). Screening for coping style increases the power of gene expression studies. PLoS ONE 4, e5314.
100. Martin, J. G. A., Nussey, D. H., Wilson, A. J. and Réale, D. (2011). Measuring individual differences in reaction norms in field and experimental studies: a power analysis of random regression models. Methods Ecol. Evol. 2, 362-374.
101. Mathot, K. J. and Dingemanse, N. J. (2015). Energetics and behavior: unrequited needs and new directions. Trends Ecol. Evol. 30, 199-206.
102. McDougall, P. T., Réale, D., Sol, D. and Reader, S. M. (2006). Wildlife conservation and animal temperament: causes and consequences of evolutionary change for captive, reintroduced, and wild populations. Anim. Conserv. 9, 39-48.
103. McGraw, K. O. and Wong, S. P. (1996). Forming inferences about some intraclass correlation coefficients. Psychol. Methods 1, 30-46.
104. Metcalfe, N. B., Van Leeuwen, T. E. and Killen, S. S. (2016). Does individual variation in metabolic phenotype predict fish behaviour and performance? J. Fish Biol. 88, 298-321.
105. Misslin, R. and Cigrang, M. (1986). Does neophobia necessarily imply fear or anxiety? Behav. Processes 12, 45-50.
106. Morrissey, M. B. and Liefting, M. (2016). Variation in reaction norms: statistical considerations and biological interpretation. Evolution 70, 1944-1959.
107. Morton, F. B., Lee, P. C. and Buchanan-Smith, H. M. (2013). Taking personality selection bias seriously in animal cognition research: a case study in capuchin monkeys (Sapajus apella). Anim. Cogn. 16, 677-684.
108. Mowles, S. L., Cotton, P. A. and Briffa, M. (2012). Consistent crustaceans: the identification of stable behavioural syndromes in hermit crabs. Behav. Ecol. Sociobiol. 66, 1087-1094.
109. Nakagawa, S. and Schielzeth, H. (2010). Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol. Rev. 85, 935-956.
110. Natarajan, D., de Vries, H., Saaltink, D.-J., de Boer, S. F. and Koolhaas, J. M. (2009). Delineation of violence from functional aggression in mice: an ethological approach. Behav. Genet. 39, 73-90.
111. Neumann, C., Agil, M., Widdig, A. and Engelhardt, A. (2013). Personality of wild male crested macaques (Macaca nigra). PLoS ONE 8, e69383.
112. Niemelä, P. T. and Dingemanse, N. J. (2014). Artificial environments and the study of 'adaptive' personalities. Trends Ecol. Evol. 29, 245-247.
113. Niemelä, P. T., Lattenkamp, E. Z. and Dingemanse, N. J. (2015). Personalityrelated survival and sampling bias in wild cricket nymphs. Behav. Ecol. 26, 936-946.
114. Norin, T., Malte, H. and Clark, T. D. (2016). Differential plasticity of metabolic rate phenotypes in a tropical fish facing environmental change. Funct. Ecol. 30, 369-378.
115. Nussey, D. H., Wilson, A. J. and Brommer, J. E. (2007). The evolutionary ecology of individual phenotypic plasticity in wild populations. J. Evol. Biol. 20, 831-844.
116. 2-induced aquatic acidification. Nature Clim. Change 5, 950-955.
117. Øverli, Ø., Sørensen, C., Pulman, K. G. T., Pottinger, T. G., Korzan, W., Summers, C. H. and Nilsson, G. E. (2007). Evolutionary background for stresscoping styles: relationships between physiological, behavioral, and cognitive traits in non-mammalian vertebrates. Neurosci. Biobehav. Rev. 31, 396-412.
118. Petelle, M. B., Martin, J. G. A. and Blumstein, D. T. (2015). Heritability and genetic correlations of personality traits in a wild population of yellow-bellied marmots (Marmota flaviventris). J. Evol. Biol. 28, 1840-1848.
119. Pike, T. W., Samanta, M., Lindström, J. and Royle, N. J. (2008). Behavioural phenotype affects social interactions in an animal network. Proc. R. Soc. B Biol. Sci. 275, 2515-2520.
120. Pollock, M. S., Clarke, L. M. J. and Dubé, M. G. (2007). The effects of hypoxia on fishes: from ecological relevance to physiological effects. Environ. Rev. 15, 1-14.
121. Réale, D., Reader, S. M., Sol, D., McDougall, P. T. and Dingemanse, N. J. (2007). Integrating animal temperament within ecology and evolution. Biol. Rev. 82, 291-318.
122. Réale, D., Dingemanse, N. J., Kazem, A. J. N. and Wright, J. (2010). Evolutionary and ecological approaches to the study of personality. Philos. Trans. R. Soc. B Biol. Sci. 365, 3937-3946.
123. Rupia, E. J., Binning, S. A., Roche, D. G. and Lu, W. (2016). Fight-flight or freezehide? Personality and metabolic phenotype mediate physiological defence responses in flatfish. J. Anim. Ecol. 85, 927-937.
124. Schuett, W., Tregenza, T. and Dall, S. R. X. (2010). Sexual selection and animal personality. Biol. Rev. 85, 217-246.
125. Sih, A., Bell, A. and Johnson, J. C. (2004a). Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol. Evol. 19, 372-378.
126. Sih, A., Bell, A. M., Johnson, J. C. and Ziemba, R. E. (2004b). Behavioral syndromes: an integrative overview. Q. Rev. Biol. 79, 241-277.
127. Sokal, R. R. and Rohlf, F. J. (1995). Biometry: The Principles and Practice of Statistics in Biological Research, 3rd edn. New York: W.H. Freeman and Company.
128. Sørensen, C., Johansen, I. B. and Øverli, Ø. (2013). Neural plasticity and stress coping in teleost fishes. Gen. Comp. Endocrinol. 181, 25-34.
129. Stamps, J. A. and Groothuis, T. G. G. (2010). Developmental perspectives on personality: implications for ecological and evolutionary studies of individual differences. Philos. Trans. R. Soc. B Biol. Sci. 365, 4029-4041.
130. Stamps, J. A., Briffa, M. and Biro, P. A. (2012). Unpredictable animals: individual differences in intraindividual variability (IIV). Anim. Behav. 83, 1325-1334.
131. Stevenson-Hinde, J., Stillwell-Barnes, R. and Zunz, M. (1980). Subjective assessment of rhesus monkeys over four successive years. Primates 21, 66-82.
132. Stuber, E. F., Araya-Ajoy, Y. G., Mathot, K. J., Mutzel, A., Nicolaus, M., Wijmenga, J. J., Mueller, J. C. and Dingemanse, N. J. (2013). Slow explorers take less risk: a problem of sampling bias in ecological studies. Behav. Ecol. 24, 1092-1098.
133. Toms, C. N., Echevarria, D. J. and Jouandot, D. J. (2010). A methodological review of personality-related studies in fish: focus on the shy-bold axis of behavior. Int. J. Comp. Psychol. 23, 1-25.
134. Tryon, R. C. (1942). Individual differences. In Comparative Psychology (ed. F. A. Moss), pp. 330-365. New York: Prentice-Hall.
135. van de Pol, M. and Wright, J. (2009). A simple method for distinguishing withinversus between-subject effects using mixed models. Anim. Behav. 77, 753-758.
136. van Noordwijk, A. J. and de Jong, G. (1986). Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128, 137-142.
137. Verbeek, M. E. M., Drent, P. J. and Wiepkema, P. R. (1994). Consistent individual differences in early exploratory behaviour of male great tits. Anim. Behav. 48, 1113-1121.
138. Videlier, M., Bonneaud, C., Cornette, R. and Herrel, A. (2014). Exploration syndromes in the frog Xenopus (Silurana) tropicalis: correlations with morphology and performance? J. Zool. 294, 206-213.
139. Westneat, D. F., Hatch, M. I., Wetzel, D. P. and Ensminger, A. L. (2011). Individual variation in parental care reaction norms: integration of personality and plasticity. Am. Nat. 178, 652-667.
140. Williams, T. D. (2008). Individual variation in endocrine systems: moving beyond the 'tyranny of the Golden Mean'. Philos. Trans. R. Soc. B Biol. Sci. 363, 1687-1698.
141. Wilson, A. D. M. and Krause, J. (2012). Personality and metamorphosis: is behavioral variation consistent across ontogenetic niche shifts? Behav. Ecol. 23, 1316-1323.
142. Wilson, D. S., Coleman, K., Clark, A. B. and Biederman, L. (1993). Shy-bold continuum in pumpkinseed sunfish (Lepomis gibbosus): an ecological study of a psychological trait. J. Comp. Psychol. 107, 250-260.
143. Wilson, D. S., Clark, A. B., Coleman, K. and Dearstyne, T. (1994). Shyness and boldness in humans and other animals. Trends Ecol. Evol. 9, 442-446.
144. Wilson, A. D. M., Brownscombe, J. W., Krause, J., Krause, S., Gutowsky, L. F. G., Brooks, E. J. and Cooke, S. J. (2015). Integrating network analysis, sensor tags, and observation to understand shark ecology and behavior. Behav. Ecol. 26, 1577-1586.
145. Wolak, M. E., Fairbairn, D. J. and Paulsen, Y. R. (2012). Guidelines for estimating repeatability. Methods Ecol. Evol. 3, 129-137.
146. Wolf, M. and Weissing, F. J. (2012). Animal personalities: consequences for ecology and evolution. Trends Ecol. Evol. 27, 452-461.
147. Zylberberg, M., Klasing, K. C. and Hahn, T. P. (2014). In house finches, Haemorhous mexicanus, risk takers invest more in innate immune function. Anim. Behav. 89, 115-122.