Context dependency of trait repeatability and its relevance for management and conservation of fish populations

Conservation Physiology

Volumn 4, Issue 1, 2016, Pages

  Killen, S S ^a   Adriaenssens, B ^a   Marras, S ^b   Claireaux, G ^c   Cooke, S J ^d  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b CNR   (Italy)

^c UNIVERSITÉ DE BRETAGNE OCCIDENTALE   (France)

^d CARLETON UNIVERSITY   (Canada)

Author keywords

Environmental effects; Intraclass correlation; Personality; Phenotypic plasticity; Reaction norm; Temperature

Indexed keywords

EID: 84983507438     PISSN: None     EISSN: 20511434     Source Type: Journal    
DOI: 10.1093/conphys/cow007     Document Type: Article

References (119)

1. Adriaenssens B, Johnsson JI (2009) Personality and life-history productivity: consistent or variable association? Trends Ecol Evol 24: 179-180.
2. Adriaenssens B, Johnsson JI (2011) Learning and context-specific exploration behaviour in hatchery and wild brown trout. Appl Anim Behav Sci 132: 90-99.
3. Adriaenssens B, Johnsson JI (2013) Natural selection, plasticity and the emergence of a behavioural syndrome in the wild. Ecol Lett 16: 47-55.
4. Angelier F, Wingfield JC (2013) Importance of the glucocorticoid stress response in a changing world: theory, hypotheses and perspectives. Gen Comp Endocrinol 190: 118-128.
5. Araya-Ajoy YG, Mathot KJ, Dingemanse NJ (2015) An approach to estimate short-term, long-term and reaction norm repeatability. Methods Ecol Evol 6: 1462-1473.
6. Archard GA, Earley RL, Hanninen AF, Braithwaite VA (2012) Correlated behaviour and stress physiology in fish exposed to different levels of predation pressure. Funct Ecol 26: 637-645.
7. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. J Stat Softw 67: 1-48.
8. Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10: 828-834.
9. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77: 771-783.
10. Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15: 365-377.
11. Bennett AF (1987) Interindividual variability: an underutilized resource. In Feder ME, Bennett AF, Burggren WW, Huey RB, eds, New Directions in Ecological Physiology. Cambridge University Press, Cambridge, pp 147-169.
12. Biro PA, Adriaenssens B (2013) Predictability as a personality trait: consistent differences in intraindividual behavioral variation. Am Nat 182: 621-629.
13. Biro PA, Stamps JA (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 25: 653-659.
14. Biro PA, Stamps JA (2015) Using repeatability to study physiological and behavioural traits: ignore time-related change at your peril. Anim Behav 105: 223-230.
15. Brommer JE (2013) Variation in plasticity of personality traits implies that the ranking of personality measures changes between environmental contexts: calculating the cross-environmental correlation. Behav Ecol Sociobiol 67: 1709-1718.
16. Careau V, Garland T Jr (2012) Performance, personality, and energetics: correlation, causation, and mechanism. Physiol Biochem Zool 85: 543-571.
17. Careau V, Thomas D, Humphries MM, Réale D (2008) Energy metabolism and animal personality. Oikos 117: 641-653.
18. Castro V, Grisdale-Helland B, Jørgensen SM, Helgerud J, Claireaux G, Farrell AP, Krasnov A, Helland SJ, Takle H (2013) Disease resistance is related to inherent swimming performance in Atlantic salmon. BMC Physiol 13: 1.
19. Chapple DG, Simmonds SM, Wong BBM (2012) Can behavioral and personality traits influence the success of unintentional species introductions? Trends Ecol Evol 27: 57-64.
20. Claireaux G, Webber DM, Lagardere J-P, Kerr SR (2000) Influence of water temperature and oxygenation on the aerobic metabolic scope of Atlantic cod (Gadus morhua). J Sea Res 44: 257-265.
21. Claireaux G, Handelsman C, Standen E, Nelson JA (2007) Thermal and temporal stability of swimming performance in the European sea bass. Physiol Biochem Zool 80: 186-196.
22. Claireaux G, Théron M, Prineau M, Dussauze M, Merlind M-X, Le Floch S (2013) Effects of oil exposure and dispersant use upon environmental adaptation performance and fitness in the European sea bass, Dicentrarchus labrax. Aquat Toxicol 130-131: 160-170.
23. Clark AB, Ehlinger TJ (1987) Patterns and adaptation in individual behavioural differences. In Bateson PPG, Klopfer PH, eds, Pespectives in Ethology, Vol 7. Plenum press, New York.
24. Cleasby I, Nakagawa S (2011) Neglected biological patterns in the residuals. Behav Ecol Sociobiol 65: 2361-2372.
25. Cleasby IR, Nakagawa S, Schielzeth H (2015) Quantifying the predictability of behaviour: statistical approaches for the study of between-individual variation in the within-individual variance. Methods Ecol Evol 6: 27-37.
26. Cockrem J (2007) Stress, corticosterone responses and avian personalities. J Ornithol 148: 169-178.
27. Cook KV, O'Connor CM, Gilmour KM, Cooke SJ (2011) The glucocorticoid stress response is repeatable between years in a wild teleost fish. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 197: 1189-1196.
28. Cook KV, O'Connor CM, McConnachie SH, Gilmour KM, Cooke SJ (2012) Condition dependent intra-individual repeatability of stress-induced cortisol in a freshwater fish. Comp Biochem Physiol A Mol Integr Physiol 161: 337-343.
29. Cooke SJ, Hinch SG, Wikelski M, Andrews RD, Kuchel LJ, Wolcott TG, Butler PJ (2004) Biotelemetry: a mechanistic approach to ecology. Trends Ecol Evol 19: 334-343.
30. Cote J, Clobert J, Brodin T, Fogarty S, Sih A (2010) Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations. Philos Trans R Soc B Biol Sci 365: 4065-4076.
31. Cripps IL, Munday PL, McCormick MI (2011) Ocean acidification affects prey detection by a predatory reef fish. PLoS ONE 6: e22736.
32. Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321: 926-929.
33. Diaz Pauli B, Wiech M, Heino M, Utne-Palm AC (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.
34. Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82: 39-54.
35. Dingemanse NJ, Wright J, Kazem AJ, Thomas DK, Hickling R, Dawnay N (2007) Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76: 1128-1138.
36. Dingemanse NJ, Kazem AJ, Réale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25: 81-89.
37. Dixson DL, Jennings AR, Atema J, Munday PL (2015) Odor tracking in sharks is reduced under future ocean acidification conditions. Glob Change Biol 21: 1454-1462.
38. Dochtermann NA, Schwab T, Sih A (2015) The contribution of additive genetic variation to personality variation: heritability of personality. Proc Biol Sci 282: 20142201.
39. Dohm M (2002) Repeatability estimates do not always set an upper limit to heritability. Funct Ecol 16: 273-280.
40. Eliason EJ, Clark TD, Hague MJ, Hanson LM, Gallagher ZS, Jeffries KM, Gale MK, Patterson DA, Hinch SG, Farrell AP (2011) Differences in thermal tolerance among sockeye salmon populations. Science 332: 109-112.
41. Ellis T, James J, Stewart C, Scott A (2004) A non-invasive stress assay based upon measurement of free cortisol released into the water by rainbow trout. J Fish Biol 65: 1233-1252.
42. Falconer DS (1981) Introduction to Quantitative Genetics. Longman, London.
43. 2 world. Oceanography 22: 36-47.
44. Ferrari MC, McCormick MI, Munday PL, Meekan MG, Dixson DL, Lönnstedt O, Chivers DP (2012) Effects of ocean acidification on visual risk assessment in coral reef fishes. Funct Ecol 26: 553-558.
45. Ferrari M, Munday PL, Rummer JL, McCormick MI, Corkill K, Watson SA, Allan BJ, Meekan MG, Chivers DP (2015) Interactive effects of ocean acidification and rising sea temperatures alter predation rate and predator selectivity in reef fish communities. Glob Change Biol 21: 1848-1855.
46. Forsythe PS, Crossman JA, Bello NM, Baker EA, Scribner KT, Tonn W (2011) Individual-based analyses reveal high repeatability in timing and location of reproduction in lake sturgeon (Acipenser fulvescens). Can J Fish Aquat Sci 69: 60-72.
47. Fry FE (1971) The effect of environmental factors on the physiology of fish. In Hoar WS, Randall DJ, eds, Fish Physiology, Vol VI. Academic Press, New York, pp 1-98.
48. Glazier DS (2005) Beyond the '3/4-power law': variation in the intra-and interspecific scaling of metabolic rate in animals. Biol Rev Camb Philos Soc 80: 611-662.
49. Hammond-Tooke CA, Nakagawa S, Poulin R (2012) Parasitism and behavioural syndromes in the fish Gobiomorphus cotidianus. Behaviour 149: 601-622.
50. Hanson KC, Cooke SJ, Hinch SG, Crossin GT, Patterson DA, English KK, Donaldson MR, Shrimpton JM, Van Der Kraak G, Farrell AP (2008) Individual variation in migration speed of upriver-migrating sockeye salmon in the Fraser river in relation to their physiological and energetic status at marine approach. Physiol Biochem Zool 81: 255-268.
51. Hanson K, Hasler C, Donaldson M, Cooke S (2010) Stability of swimming performance and activity hierarchies among wild largemouth bass at multiple temporal scales: evidence for context-dependent shuffling between seasons. Can J Zool 88: 324-333.
52. Harrison PM, Gutowsky LFG, Martins EG, Patterson DA, Cooke SJ, Power M (2015) Personality-dependent spatial ecology occurs independently from dispersal in wild burbot (Lota lota). Behav Ecol 26: 483-492.
53. Holmlund CM, Hammer M (1999) Ecosystem services generated by fish populations. Ecol Econ 29: 253-268.
54. Horodysky AZ, Cooke SJ, Brill RW (2015) Physiology in the service of fisheries science: why thinking mechanistically matters. Rev Fish Biol Fish 25: 425-447.
55. Huntingford FA (1976) The relationship between inter-and intra-specific aggression. Anim Behav 24: 485-497.
56. Johnson PCD, Barry SJE, Ferguson HM, Müller P (2015) Power analysis for generalized linear mixed models in ecology and evolution. Methods Ecol Evol 6: 133-142.
57. Johnston I, Wilson RS (2006) Temperature-induced developmental plasticity in ectotherms. In SJ Warburton, Burggren WW, Pelster B, Reiber CL, Spicer J, eds, Comparative Developmental Physiology, Oxford University Press, New York, pp 124-138.
58. Jornod M, Roche DG (2015) Inter-vs intra-individual variation and temporal repeatability of escape responses in the coral reef fish Amblyglyphidodon curacao. Biology Open 4: 1395-1399.
59. Joyce W, Ozolina K, Mauduit F, Ollivier H, Claireaux G, Shiels HA (2016) Individual variation in whole-animal hypoxia tolerance is associated with cardiac hypoxia tolerance in a marine teleost. Biol Lett 12: 20150708.
60. Killen SS (2014) Growth trajectory influences temperature preference in fish through an effect on metabolic rate. J Anim Ecol 83: 1513-1522.
61. Killen SS, Marras S, McKenzie DJ (2011) Fuel, fasting, fear: routine metabolic rate and food deprivation exert synergistic effects on risk taking in individual juvenile European seabass. J Anim Ecol 80: 1024-1033.
62. Killen SS, Marras S, Ryan MR, Domenici P, McKenzie DJ (2012a) A relationship between metabolic rate and risk-taking behaviour is revealed during hypoxia in juvenile European sea bass. Funct Ecol 26: 134-143.
63. Killen SS, Marras S, Steffensen JF, McKenzie DJ (2012b) Aerobic capacity influences the spatial position of individuals within fish schools. Proc Biol Sci 279: 357-364.
64. Killen SS, Marras S, Metcalfe NB, McKenzie DJ, Domenici P (2013) Environmental stressors alter relationships between physiology and behaviour. Trends Ecol Evol 28: 651-658.
65. Killen SS, Marras S, McKenzie DJ (2014) Fast growers sprint slower: effects of food deprivation and re-feeding on sprint swimming performance in individual juvenile European sea bass. J Exp Biol 217: 859-865.
66. Killen SS, Nati JJH, Suski CD (2015) Vulnerability of individual fish to capture by trawling is influenced by capacity for anaerobic metabolism. Proc Biol Sci 282: 20150603.
67. Killen SS, Fu C, Wu Q, Wang YX, Fu SJ (2016) The relationship between metabolic rate and sociability is altered by food deprivation. Funct Ecol. DOI:10.1111/1365-2435.12634
68. Kolok AS (1992) The swimming performance of individual largemouth bass (Micropterus salmoides) are repeatable. J Exp Biol 170: 265-270.
69. Kolok AS, Plaisance EP, Abdelghani A (1998) Individual variation in the swimming performance of fishes: an overlooked source of variation in toxicity studies. Environ Toxicol Chem 17: 282-285.
70. Koolhaas JM (2008) Coping style and immunity in animals: making sense of individual variation. Brain Behav Immun 22: 662-667.
71. Koukkari WL, Sothern RB (2007) Introducing Biological Rhythms: a Primer on the Temporal Organization of Life, with Implications for Health, Society, Reproduction, and the Natural Environment. Springer Science & Business Media, Springer, Netherlands.
72. Krause J (1993) The influence of hunger on shoal size choice by threespined sticklebacks, Gasterosteus aculeatus. J Fish Biol 43: 775-780.
73. Krause J, Cheng DJS, Kirkman E, Ruxton GD (2000) Species-specific patterns of refuge use in fish: the role of metabolic expenditure and body length. Behaviour 137: 1113-1127.
74. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104: 116-121.
75. Maciak S, Konarzewski M (2010) Repeatability of standard metabolic rate (SMR) in a small fish, the spined loach (Cobitis taenia). Comp Biochem Physiol A Mol Integr Physiol 157: 136-141.
76. McKenzie DJ, Piraccini G, Steffensen JF, Bolis CL, Bronzi P, Taylor EW (1995) Effects of diet on spontaneous locomotor activity and oxygen consumption in Adriatic sturgeon (Acipenser naccarii). Fish Physiol Biochem 14: 341-355.
77. Magurran AE (1986) Individual differences in fish behaviour. In Pitcher T, ed., The Behaviour of Teleost Fishes. Springer, USA, pp 338-365.
78. Marras S, Killen SS, Claireaux G, Domenici P, McKenzie DJ (2011) Behavioural and kinematic components of the fast-start escape response in fish: individual variation and temporal repeatability. J Exp Biol 214: 3102-3110.
79. Marras S, Cucco A, Antognarelli F, Azzurro E, Milazzo M, Bariche M, Butenschön M, Kay S, Di Bitetto M, Quattrocchi G et al. (2015a) Predicting future thermal habitat suitability of competing native and invasive fish species: from metabolic scope to oceanographic modelling. Conserv Physiol 3: doi:10.1093/conphys/cou059.
80. Marras S, Killen SS, Lindström J, McKenzie DJ, Steffensen JF, Domenici P (2015b) Fish swimming in schools save energy regardless of their spatial position. Behav Ecol Sociobiol 69: 219-226.
81. Martin JG, Nussey DH, Wilson AJ, Reale 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.
82. Martinez M, Guderley H, Nelson JA, Webber D, Dutil JD (2002) Once a fast cod, always a fast cod: maintenance of performance hierarchies despite changing food availability in cod (Gadus morhua). Physiol Biochem Zool 75: 90-100.
83. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16: 254-260.
84. Metcalfe NB, Van Leeuwen TE, Killen SS (2016) Does individual variation in metabolic phenotype predict fish behaviour and performance? J Fish Biol 88: 298-321.
85. Mittelbach GG, Ballew NG, Kjelvik MK (2014) Fish behavioral types and their ecological consequences. Can J Fish Aquat Sci 71: 927-944.
86. Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS, Devitsina GV, Doving KB (2009) Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc Natl Acad Sci USA 106: 1848-1852.
87. Nagy M, Akos Z, Biro D, Vicsek T (2010) Hierarchical group dynamics in pigeon flocks. Nature 464: 890-893.
88. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev Camb Philos Soc 85: 935-956.
89. Nelson JA, Gotwalt PS, Simonetti CA, Snodgrass JW (2008) Environmental correlates, plasticity, and repeatability of differences in performance among blacknose dace (Rhinichthys atratulus) populations across a gradient of urbanization. Physiol Biochem Zool 81: 25-42.
90. Nelson JA, Atzori F, Gastrich KR (2015) Repeatability and phenotypic plasticity of fish swimming performance across a gradient of urbanization. Environ Biol Fish 98: 1431-1447.
91. Nespolo RF, Franco M (2007) Whole-animal metabolic rate is a repeatable trait: a meta-analysis. J Exp Biol 210: 2000-2005.
92. Norin T, Malte H (2011) Repeatability of standard metabolic rate, active metabolic rate and aerobic scope in young brown trout during a period of moderate food availability. J Exp Biol 214: 1668-1675.
93. Norin T, Malte H, Clark TD (2015) Differential plasticity of metabolic rate phenotypes in a tropical fish facing environmental change. Funct Ecol DOI:10.1111/1365-2435.12503.
94. Nussey D, Wilson A, Brommer J (2007) The evolutionary ecology of individual phenotypic plasticity in wild populations. J Evol Biol 20: 831-844.
95. Oomen RA, Hutchings JA (2015) Variation in spawning time promotes genetic variability in population responses to environmental change in a marine fish. Conserv Physiol 3: doi:10.1093/conphys/cov027.
96. Philipp DP, Cooke SJ, Claussen JE, Koppelman JB, Suski CD, Burkett DP (2009) Selection for vulnerability to angling in largemouth bass. Trans Am Fish Soc 138: 189-199.
97. R Core Team (2015) R: A Language and Environment for Statistical Computing. R, Foundation for Statistical Computing, Vienna, Austria.
98. Sandblom E, Djordjevic B, Sundh H, Seth H, Sundell K, Lines JA, Kiessling A (2012) Effects of electric field exposure on blood pressure, cardioventilatory activity and the physiological stress response in Arctic char, Salvelinus alpinus. Aquaculture 344-349: 135-140.
99. Schielzeth H, Forstmeier W (2009) Conclusions beyond support: overconfident estimates in mixed models. 20: 416-420.
100. Sih A (2013) Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Anim Behav 85: 1077-1088.
101. Slater PJB (1981) Individual differences in animal behavior. In Bateson P, Klopfer P, eds, Perspectives in Ethology. Springer, USA, pp 35-49.
102. Sloman KA, Motherwell G, O'Connor KI, Taylor AC (2000) The effect of social stress on the standard metabolic rate (SMR) of brown trout, Salmo trutta. Fish Physiol Biochem 23: 49-53.
103. Sneddon LU, Hawkesworth S, Braithwaite VA, Yerbury J (2006) Impact of environmental disturbance on the stability and benefits of individual status within dominance hierarchies. Ethology 112: 437-447.
104. Sprenger D, Dingemanse NJ, Dochtermann NA, Theobald J, Walker SPW (2012) Aggressive females become aggressive males in a sex-changing reef fish. Ecol Lett 15: 986-992.
105. Stamps JA, Briffa M, Biro PA (2012) Unpredictable animals: individual differences in intraindividual variability (IIV). Anim Behav 83: 1325-1334.
106. Svendsen JC, Genz J, Anderson WG, Stol JA, Watkinson DA, Enders EC (2014) Evidence of circadian rhythm, oxygen regulation capacity, metabolic repeatability and positive correlations between forced and spontaneous maximal metabolic rates in lake sturgeon Acipenser fulvescens. PLoS ONE 9: e94693.
107. Svendsen MBS, Bushnell PG, Steffensen JF (2016) Design and setup of intermittent-flow respirometry system for aquatic organisms. J Fish Biol 88: 26-50.
108. Taylor M, Cooke S (2014) Repeatability of movement behaviour in a wild salmonid revealed by telemetry. J Fish Biol 84: 1240-1246.
109. Van Leeuwen TE, Rosenfeld JS, Richards JG (2012) Effects of food ration on SMR: influence of food consumption on individual variation in metabolic rate in juvenile coho salmon (Onchorhynchus kisutch). J Anim Ecol 81: 395-402.
110. Virani NA, Rees BB (2000) Oxygen consumption, blood lactate and interindividual variation in the gulf killifish, Fundulus grandis, during hypoxia and recovery. Comp Biochem Physiol A Mol Integr Physiol 126: 397-405.
111. Wang T, Hung CCY, Randall DJ (2006) The comparative physiology of food deprivation: from feast to famine. Annu Rev Physiol 68: 223-251.
112. West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 249-278.
113. Westneat DF, Wright J, Dingemanse NJ (2015) The biology hidden inside residual within-individual phenotypic variation. Biol Rev Camb Philos Soc 90: 729-743.
114. White JR, McCormick MI, Meekan MG (2013) Syndromes or flexibility: behavior during a life history transition of a coral reef fish. PLoS ONE 8: e84262.
115. White JR, Meekan MG, McCormick MI (2015) Individual consistency in the behaviors of newly-settled reef fish. PeerJ 3: e961.
116. Williams TD (2008) Individual variation in endocrine systems: moving beyond the 'tyranny of the golden mean'. Philos Trans R Soc B Biol Sci 363: 1687-1698.
117. Wilson ADM, Binder TR, McGrath KP, Cooke SJ, Godin J-GJ (2011) Capture technique and fish personality: angling targets timid bluegill sunfish, Lepomis macrochirus. Can J Fish Aquat Sci 68: 749-757.
118. Wingfield JC (2003) Control of behavioural strategies for capricious environments. Anim Behav 66: 807-816.
119. Wolak ME, Fairbairn DJ, Paulsen YR (2012) Guidelines for estimating repeatability. Methods Ecol Evol 3: 129-137.