Individual (Co)variation in standard metabolic rate, feeding rate, and exploratory behavior in wild-caught semiaquatic salamanders

Physiological and Biochemical Zoology

Volumn 87, Issue 3, 2014, Pages 384-396

  Gifford, Matthew E ^a   Clay, Timothy A ^a   Careau, Vincent ^b  

^a University of Arkansas   (United States)

^b DEAKIN UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BEHAVIORAL ECOLOGY; BODY MASS; CORRELATION; FEEDING BEHAVIOR; GENETIC ANALYSIS; METABOLISM; PHENOTYPIC PLASTICITY; REPTILE;

ANIMAL; BASAL METABOLIC RATE; BODY WEIGHT; EATING; ENERGY METABOLISM; EXPLORATORY BEHAVIOR; FEEDING BEHAVIOR; METABOLISM; PHENOTYPE; PHYSIOLOGY; URODELA;

ANIMALS; BASAL METABOLISM; BODY WEIGHT; EATING; ENERGY METABOLISM; EXPLORATORY BEHAVIOR; FEEDING BEHAVIOR; PHENOTYPE; URODELA;

EID: 84899629979     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/675974     Document Type: Article

References (71)

1. Angilletta M.J., Jr., A.F. Bennett, H. Guderley, C.A. Navas, F. Seebacher, and R.S. Wilson. 2006. Coadaptation: a unifying principle in evolutionary thermal biology. Physiol Biochem Zool 79:282-294.
2. Arnold S.J. 1983. Morphology, performance and fitness. Am Zool 23:347-361.
3. Austin C.C. and H.B. Shaffer. 1992. Short-term, medium-term, and long-term repeatability of locomotor performance in the tiger salamander Ambystoma californiense. Funct Ecol 6:145- 153.
4. Avgar T., N. Horvitz, L. Broitman, and R. Nathan. 2008. How movement properties affect prey encounter rates of ambush versus active predators: a comment on Scharf et al. Am Nat 172:593-595.
5. Bauwens D., T. Garland, A.M. Castilla, and R. Vandamme. 1995. Evolution of sprint speed in lacertid lizards: morphological, physiological, and behavioral covariation. Evolution 49:848-863.
6. Bell A.M., S.J. Hankison, and K.L. Laskowski. 2009. The repeatability of behaviour: a meta-analysis. Anim Behav 77: 771-783.
7. Bennett A.F. 1987. Interindividual variability: an underutilized resource. Pp. 147-169 in M.E. Feder, A.F. Bennett, W.W. Burggren, and R.B. Huey, eds. New directions in ecological physiology. Cambridge University Press, Cambridge.
8. Biro P.A. and J.A. Stamps. 2010. Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 24:653-659.
9. Boake C.R. 1989. Repeatability: its role in evolutionary studies of mating behavior. Evol Ecol 3:173-182.
10. Boake C.R. 1994. Quantitative genetic studies of behavioral evolution. University of Chicago Press, Chicago.
11. Boon A.K., D. Reale, and S. Boutin. 2008. Personality, habitat use, and their consequences for survival in North American red squirrels Tamiasciurus hudsonicus. Oikos 117:1321-1328.
12. Bouwhuis S., J.L. Quinn, B.C. Sheldon, and S. Verhulst. 2013. Personality and basal metabolic rate in a wild bird population. Oikos 123:56-62.
13. Boyer N., D. Réale, J. Marmet, B. Pisanu, and J.L. Chapuis. 2010. Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. J Anim Ecol 79:538-547.
14. Broggi J., E. Hohtola, K. Koivula, M. Orell, and J.A. Nilsson. 2009. Long-term repeatability of winter basal metabolic rate and mass in a wild passerine. Funct Ecol 23:768-773.
15. 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.
16. Burton T., S.S. Killen, J.D. Armstrong, and N.B. Metcalfe. 2011. What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proc R Soc B 278: 3465-3473.
17. Butler D., B.R. Cullis, A.R. Gilmour, and D.J. Gogel. 2007. ASReml-R reference manual, release 2.0. VSN International, Hemel Hempstead, UK.
18. Calsbeek R., S.H. Alonzo, K. Zamudio, and B. Sinervo. 2002. Sexual selection and alternative mating behaviours generate demographic stochasticity in small populations. Proc R Soc B 269:157-164.
19. Careau V., O.R.P. Bininda-Emonds, D. Thomas, M.M. Humphries, and D. Réale. 2009. Exploration strategies map along fast-slow metabolic and life-history continua in muroid rodents. Funct Ecol 23:150-156.
20. Careau V. and T. Garland Jr. 2012. Performance, personality, and energetics: correlation, causation, and mechanism. Phys-iol Biochem Zool 85:543-571.
21. Careau V., D. Thomas, M.M. Humphries, and D. Réale. 2008. Energy metabolism and animal personality. Oikos 117:641- 653.
22. Careau V., D. Thomas, F. Pelletier, L. Turki, F. Landry, D. Gar-ant, and D. Réale. 2011. Genetic correlation between resting metabolic rate and exploratory behaviour environment in deer mice (Peromyscus maniculatus). J Evol Biol 24:2153- 2163.
23. Chappell M.A., G.C. Bachman, and J.P. Odell. 1995. Repeatability of maximal aerobic performance in Belding's ground squirrels, Spermophilus beldingi. Funct Ecol 9:498-504.
24. Chappell M.A., M. Zuk, and T.S. Johnsen. 1996. Repeatability of aerobic performance in red junglefowl: effects of ontogeny and nematode infection. Funct Ecol 10:578-585.
25. Corl A., A.R. Davis, S.R. Kuchta, T. Comendant, and S. Sinervo. 2010. Alternative mating strategies and the evolution of sex ual size dimorphism in the side-blotched lizard, Uta stans- buriana: a population-level comparative analysis. Evolution 64:79-96.
26. De Vera L. and J.P. Hayes. 1995. Repeatability of oxygen consumption in Gallotia galloti. J Herpetol 29:151-154.
27. Dingemanse N.J., C. Both, A.J. van Noordwijk, A.L. Rutten, and P.J. Drent. 2003. Natal dispersal and personalities in grea t tits (Parus major). Proc R Soc B 270:741-747.
28. Dingemanse N.J., K.M. Bouwman, M. van de Pol, T. van Overveld, S.C. Patrick, E. Matthysen, and J.L. Quinn. 2012a. Variation in personality and behavioural plasticity across four populations of the great tit Parus major. J Anim Ecol 81: 116-126.
29. Dingemanse N.J. and N.A. Dochtermann. 2013. Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39-54.
30. Dingemanse N.J., N.A. Dochtermann, and S. Nakagawa. 2012b. Defining behavioural syndromes and the role of "syndrome deviation" in understanding their evolution. Behav Ecol So-ciobiol 66:1543-1548.
31. Dingemanse N.J. and D. Reale. 2005. Natural selection and animal personality Behaviour 142:1159-1184.
32. Dingemanse N.J., J. Wright, A.J.N. Kazem, D.K. Thomas, R. Hickling, and N. Dawnay 2007. Behavioural syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128-1138.
33. Dohm M.R. 2002. Repeatability estimates do not always set an upper limit to heritability Funct Ecol 16:273-280.
34. Dominicus A., A. Skrondal, H.K. Gjessing, NL. Pedersen, and J. Palmgren. 2006. Likelihood ratio tests in behavioral genetics: problems and solutions. Behav Genet 36:331-340.
35. Falconer D.S. and T.F.C. Mackay 1996. Introduction to quantitative genetics. 4th ed. Longman, Harlow.
36. Ferrari C, C. Pasquaretta, C. Carere, E. Cavallone, A. von Hardenberg, and D. Reale. 2013. Testing for the presence of coping styles in a wild mammal. Anim Behav 85:1385-1396.
37. Fraser D.F., J.F. Gilliam, M.J. Daley, N. Le An, and T.S. Garrick. 2001. Explaining leptokurtic movement distributions: intra-population variation in boldness and exploration. Am Nat 158:124-135.
38. Garland T, Jr., and J.B. Losos. 1994. Ecological morphology of locomotor performance in squamate reptiles. Pp. 240-302 in P.C. Wainwright and S.M. Reilly, eds. Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago.
39. Kenward M.G. and J.H. Roger. 1997. The precision of fixed effects estimates from restricted maximum likelihood. Biometrics 53:983-997.
40. Kruuk L.E.B., T.H. Clutton-Brock, J. Slate, J.M. Pemberton, S. Brotherstone, and F.E. Guinness. 2000. Heritability of fitness in a wild mammal population. Proc Natl Acad USA 97:698-703.
41. Lantova P., K. Zub, K. Sľchova, and Z. Borowski. 2011. Linkages between metabolism and personality in small mammals: the root vole (Microtus oeconomus) example. Physiol Behav 104: 378-383.
42. Le Galliard J.-F., M. Paquet, M. Cisel, and L. Montes-Poloni. 2012. Personality and the pace of-life syndrome: variation and selection on exploration, metabolism and locomotor performances. Funct Ecol 27:136-144.
43. Lynch M. and J.B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland, MA.
44. Maldonado K., W.F.D. van Dongen, R.A. Vásquez, and P. Sabat. 2012. Geographic variation in the association between exploratory behavior and physiology in rufous-collared sparrows. Physiol Biochem Zool 85:618-624.
45. Martin J.G.A. and D. Réale. 2008. Temperament, risk assessment and habituation to novelty in eastern chipmunks, Ta m -ias striatus. Anim Behav 75:309-318.
46. Martin L.B., D. Hasselquist, and M. Wikelski. 2006. Investment in immune defense is linked to pace of life in house sparrows. Oecologia 147:565-575.
47. Mettke-Hofmann C., H. Winkler, and B. Leisler. 2002. The significance of ecological factors for exploration and neo-phobia in parrots. Ethology 108:249-272.
48. Montiglio P.O., D. Garant, F. Pelletier, and D. Réale. 2012. Personality differences are related to long-term stress reactivity in a population of wild eastern chipmunks, Tamias striatus. Anim Behav 84:1071-1079.
49. Mousseau T.A. and D.A. Roff. 1987. Natural selection and the heritability of fitness components. Heredity 59:181-197.
50. Nespolo R.F. and M. Franco. 2007. Whole-animal metabolic rate is a repeatable trait: a meta-analysis. J Exp Biol 210: 2000-2005.
51. Nilsson J.A. 2002. Metabolic consequences of hard work. Proc R Soc B 269:1735-1739.
52. Norin T. and H. Malte. 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.
53. O'Connor K.I., A.C. Taylor, and N.B. Metcalfe. 2000. The stability of standard metabolic rate during a period of food deprivation in juvenile Atlantic salmon. J Fish Biol 57:41-51.
54. Réale D., D. Garant, M.M. Humphries, P. Bergeron, V. Careau, and P.O. Montiglio. 2010. Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos Trans R Soc B 365:4051-4063.
55. Ricklefs R.E. and M. Wikelski. 2002. The physiology/life-history nexus. Trends Ecol Evol 17:462-468.
56. Sadowska E.T., K. Baliga-Klimczyk, M.K. Labocha, and P. Ko-teja. 2009. Genetic correlations in a wild rodent: grass-eaters and fast-growers evolve high basal metabolic rates. Evolution 63:1530-1539.
57. Self S.C. and K.Y. Liang. 1987. Asymptotic properties of maximum likelihood estimators and likelihood ratio tests under non-standard conditions. J Am Stat Soc 82:605-610.
58. Singer J.D. and J.B. Willett. 2003. Applied longitudinal data analysis: modeling change and event occurrence. Oxford University Press, New York.
59. Stirling D.G., D. Réale, and D.A. Roff. 2002. Selection, structure and the heritability of behaviour. J Evol Biol 15:277-289.
60. Timonin M.E., C.J. Carriére, A.D. Dudych, J.G.W. Latimer, S.T. Unruh, and C.K.R. Wilis. 2011. Individual differences in the behavioural responses of meadow voles (Microtus pennsyl-vanicus) to an unfamiliar environment are not correlated with variation in resting metabolic rate. J Zool 284:198-205.
61. van Overveld T. and E. Matthysen. 2010. Personality predicts spatial responses to food manipulations in free ranging great tits (Parus major). Biol Lett 6:187-190.
62. Versteegh M.A., B. Heim, N.J. Dingemanse, and B.I. Tieleman. 2008. Repeatability and individual correlates of basal metabolic rate and total evaporative water loss in birds: a case study in European stonechats. Comp Biochem Physiol A150: 452-457.
63. Walsh B. and M.W. Blows. 2009. Abundant genetic variation + strong selection p multivariate genetic constraints: a geometric view of adaptation. Ann Rev Ecol Evol Syst 40:41-59.
64. White C.R., N.G. Schimpf, and P. Cassey. 2013. The repeatability of metabolic rate declines with time. J Exp Biol 216: 1763-1765.
65. Wikelski M., L. Spinney, W. Schelsky, A. Scheuerlein, and E. Gwinner. 2003. Slow pace of life in tropical sedentary birds: a common-garden experiment on four stonechat populations from different latitudes. Proc R Soc B 270:2383-2388.
66. 2 does not always equal VA/VP? J Evol Biol 21:647-650.
67. Wilson D.S. 1998. Adaptive individual differences within single populations. Philos Trans R Soc B 353:199-205.
68. Wilson D.S., A.B. Clark, K. Coleman, and T. Dearstyne. 1994. Shyness and boldness in humans and other animals. Trends Ecol Evol 9:442-446.
69. Withers P.C. 2001. Design, calibration and calculation for flow-through respirometry systems. Aust J Zool 49:445-461.
70. Wolak M.E., D.J. Fairbairn, and Y.R. Paulsen. 2012. Guidelines for estimating repeatability. Methods Ecol Evol 3:129-137.
71. Zollner P.A. and S.L. Lima. 1999. Search strategies for landscape-level interpatch movements. Ecology 80:1019-1030.