A relationship between metabolic rate and risk-taking behaviour is revealed during hypoxia in juvenile European sea bass

Functional Ecology

Volumn 26, Issue 1, 2012, Pages 134-143

  Killen, Shaun S ^a,b   Marras, Stefano ^a,c   Ryan, Mary R ^b   Domenici, Paolo ^d   Mckenzie, David J ^a  

^a INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c IMC International Marine Centre   (Italy)

^d CNR   (Italy)

Author keywords

Boldness; Ecophysiology; Foraging; Personality; Physiological energetics; Predation; Teleost fish

Indexed keywords

DISEASE SEVERITY; ECOPHYSIOLOGY; ENERGETICS; FORAGING BEHAVIOR; HYPOXIA; JUVENILE; METABOLISM; OXYGEN; PHYSIOLOGICAL RESPONSE; RESPIRATION; SWIMMING BEHAVIOR; TELEOST;

ANIMALIA; DICENTRARCHUS LABRAX; TELEOSTEI;

EID: 84856007958     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2011.01920.x     Document Type: Article

References (56)

1. Addis, P. & Cau, A. (1997) Impact of the feeding habits of the great cormorant Phalacrocorax carbo sinensis on the lagoon fish stocks in central western Sardinia. Avocetta, 21, 180-187.
2. Álvarez, D. & Nicieza, A.G. (2005) Is metabolic rate a reliable predictor of growth and survival of brown trout (Salmo trutta) in the wild? Canadian Journal of Fisheries and Aquatic Sciences, 62, 643-649.
3. Biro, P.A. & Stamps, J.A. (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends in Ecology & Evolution, 25, 653-659.
4. Bochdansky, A., Grønkjær, P., Herra, T. & Leggett, W. (2005) Experimental evidence for selection against fish larvae with high metabolic rates in a food limited environment. Marine Biology, 147, 1413-1417.
5. Broggi, J., Hohtola, E., Koivula, K., Orell, M. & Nilsson, J.-Å. (2009) Long-term repeatability of winter basal metabolic rate and mass in a wild passerine. Functional Ecology, 23, 768-773.
6. Bushnell, P.G., Steffensen, J.F. & Johansen, K. (1984) Oxygen consumption and swimming performance in hypoxia-acclimated rainbow trout Salmo gairdneri. Journal of Experimental Biology, 113, 225-235.
7. Careau, V., Thomas, D., Humphries, M.M. & Réale, D. (2008) Energy metabolism and animal personality. Oikos, 117, 641-653.
8. Chabot, D. & Claireaux, G. (2008) Environmental hypoxia as a metabolic constraint on fish: the case of Atlantic cod, Gadus morhua. Marine Pollution Bulletin, 57, 287-294.
9. Chapman, L.J. & McKenzie, D.J. (2009) Chapter 2 Behavioral responses and ecological consequences. Fish Physiology (eds D.A.P.F. Jeffrey, G. Richards & J.B. Colin ), pp. 25-77, Academic Press, San Diego, California, USA.
10. Coleman, K. & Wilson, D.S. (1998) Shyness and boldness in pumpkinseed sunfish are context-specific. Animal Behaviour, 56, 927-936.
11. Cutts, C.J., Metcalfe, N.B. & Taylor, A.C. (1998) Aggression and growth depression in juvenile Atlantic salmon: the consequences of individual variation in standard metabolic rate. Journal of Fish Biology, 52, 1026-1037.
12. Diaz, R.J. & Rosenberg, R. (2008) Spreading dead zones and consequences for marine ecosystems. Science, 321, 926-929.
13. Dingemanse, N.J., Kazem, A.J.N., Réale, D. & Wright, J. (2009) Behavioural reaction norms: animal personality meets individual plasticity. Trends in Ecology & Evolution, 25, 81-89.
14. Di-Poï, C., Attia, J., Bouchut, C., Dutto, G., Covès, D. & Beauchaud, M. (2007) Behavioral and neurophysiological responses of European sea bass groups reared under food constraint. Physiology & Behavior, 90, 559-566.
15. Domenici, P., Steffensen, J.F. & Batty, R.S. (2000) The effect of progressive hypoxia on swimming activity and schooling in Atlantic herring. Journal of Fish Biology, 57, 1526-1538.
16. Dupont-Prinet, A., Claireaux, G. & McKenzie, D.J. (2009) Effects of feeding and hypoxia on cardiac performance and blood flow allocation during aerobic exercise in the European sea bass Dicentrarchus labrax. Comparative Biochemistry and Physiology, 154, 233-240.
17. Dupont-Prinet, A., Chatain, B., Grima, L., Vandeputte, M., Claireaux, G. & McKenzie, D.J. (2010) Physiological mechanisms underlying a trade-off between growth rate and tolerance of feed deprivation in the European sea bass (Dicentrarchus labrax). Journal of Experimental Biology, 213, 1143-1152.
18. Finstad, A.G., Forseth, T., Ugedal, O. & Naesje, T.F. (2007) Metabolic rate, behaviour and winter performance in juvenile Atlantic salmon. Functional Ecology, 21, 905-912.
19. Giske, J., Huse, G. & Fiksen, O. (1998) Modelling spatial dynamics of fish. Reviews in Fish Biology and Fisheries, 8, 57-91.
20. Godin, J.-G.J. & Smith, S.A. (1988) A fitness cost of foraging in the guppy. Nature, 333, 69-71.
21. Huntingford, F.A., Andrew, G., MacKenzie, S., Morera, D., Coyle, S.M., Pilarczyk, M. & Kadri, S. (2010) Coping strategies in a strongly schooling fish, the common carp Cyprinus carpio. Journal of Fish Biology, 76, 1576-1591.
22. Jobling, M. (1994) Fish Bioenergetics. Chapman & Hall, London.
23. Kersten, M., Britton, R.H., Dugan, P.J. & Hafner, H. (1991) Flock feeding and food intake in little egrets: the effects of prey distribution and behaviour. Journal of Animal Ecology, 60, 241-252.
24. Killen, S.S., Marras, S. & McKenzie, D.J. (2011) Fuel, fasting, fear: routine metabolic rate and food deprivation exert synergistic effects on risk-taking in individual juvenile European sea bass. Journal of Animal Ecology, 80, 1024-1033.
25. Kramer, D. (1987) Dissolved oxygen and fish behavior. Environmental Biology of Fishes, 18, 81-92.
26. Kramer, D., Manley, D. & Bourgeois, R. (1983) The effect of respiratory mode and oxygen concentration on the risk of aerial predation in fishes. Canadian Journal of Fisheries and Aquatic Sciences, 61, 653-665.
27. Krause, J., Loader, S.P., McDermott, J. & Ruxton, G.D. (1998) Refuge use by fish as a function of body length related metabolic expenditure and predation risks. Proceedings of the Royal Society of London. Series B: Biological Sciences, 265, 2373-2379.
28. Lefrançois, C., Ferrari, R.S., Moreira Da Silva, J. & Domenici, P. (2009) The effect of progressive hypoxia on spontaneous activity in single and shoaling golden grey mullet Liza aurata. Journal of Fish Biology, 75, 1615-1625.
29. Magurran, A.E. & Girling, S.L. (1986) Predator model recognition and response habituation in shoaling minnows. Animal Behaviour, 34, 510-518.
30. Marras, S., Claireaux, G., McKenzie, D.J. & Nelson, J.A. (2010) Individual variation and repeatability in aerobic and anaerobic swimming performance of European sea bass, Dicentrarchus labrax. Journal of Experimental Biology, 213, 26-32.
31. Martel, G. & Dill, L.M. (1995) Influence of movement by coho salmon (Oncorhynchus kisutch) parr on their detection by common mergansers (Mergus merganser). Ethology, 99, 139-149.
32. Martins, C.I.M., Castanheira, M.F., Engrola, S., Costas, B. & Conceição, L.E.C. (2011) Individual differences in metabolism predict coping styles in fish. Applied Animal Behaviour Science, 130, 135-143.
33. McCarthy, I.D. (2000) Temporal repeatability of relative standard metabolic rate in juvenile Atlantic salmon and its relation to life history variation. Journal of Fish Biology, 57, 224-238.
34. McCarthy, I.D. (2001) Competitive ability is related to metabolic asymmetry in juvenile rainbow trout. Journal of Fish Biology, 59, 1002-1014.
35. Metcalfe, N.B., Taylor, A.C. & Thorpe, J.E. (1995) Metabolic rate, social status and life-history strategies in Atlantic salmon. Animal Behaviour, 49, 431-436.
36. Millidine, K.J., Metcalfe, N.B. & Armstrong, J.D. (2009) Presence of a conspecific causes divergent changes in resting metabolism, depending on its relative size. Proceedings of the Royal Society B: Biological Sciences, 276, 3989-3993.
37. Nespolo, R.F. & Franco, M. (2007) Whole-animal metabolic rate is a repeatable trait: a meta-analysis. Journal of Experimental Biology, 210, 2000-2005.
38. Nilsson, G.E. & Östlund-Nilsson, S. (2008) Does size matter for hypoxia tolerance in fish? Biological Reviews, 83, 173-189.
39. Priede, I.G. (1985) Metabolic scope in fishes. Croom-Helm, London.
40. Quinn, G. & Keough, M. (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge.
41. Réale, D., Reader, S.M., Sol, D., Mcdougall, P.T. & Dingemanse, N.J. (2007) Integrating animal temperament within ecology and evolution. Biological Reviews, 82, 291-318.
42. Robb, T. & Abrahams, M.V. (2003) Variation in tolerance to hypoxia in a predator and prey species: an ecological advantage of being small? Journal of Fish Biology, 62, 1067-1081.
43. Rodnick, K.J., Gamperl, A.K., Lizars, K.R., Bennett, M.T., Rausch, R.N. & Keeley, E.R. (2004) Thermal tolerance and metabolic physiology among redband trout populations in south-eastern Oregon. Journal of Fish Biology, 64, 310-335.
44. Schurmann, H. & Steffensen, J.F. (1994) Spontaneous swimming activity of Atlantic cod Gadus mohua exposed to graded hypoxia at three temperatures. Journal of Experimental Biology, 197, 129-142.
45. Shingles, A., McKenzie, D.J., Claireaux, G. & Domenici, P. (2005) Reflex cardioventilatory responses to hypoxia in the flathead gray mullet (Mugil cephalus) and their behavioral modulation by perceived threat of predation and water turbidity. Physiological and Biochemical Zoology, 78, 744-755.
46. Sih, A., Bell, A. & Johnson, J.C. (2004) Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology & Evolution, 19, 372-378.
47. Skelly, D.K. (1994) Activity level and the susceptibility of anuran larvae to predation. Animal Behaviour, 47, 465-468.
48. Sloman, K.A., Motherwell, G., O'Connor, K.I. & Taylor, A.C. (2000) The effect of social stress on the standard metabolic rate (SMR) of brown trout, Salmo trutta. Fish Physiology and Biochemistry, 23, 49-53.
49. Sloman, K.A., Wood, C.M., Scott, G.R., Wood, S., Kajimura, M., Johannsson, O.E., Almeida-Val, V.M.F. & Val, A.L. (2006) Tribute to R. G. Boutilier: The effect of size on the physiological and behavioural responses of oscar, Astronotus ocellatus, to hypoxia. Journal of Experimental Biology, 209, 1197-1205.
50. Sokal, R.R. & Rohlf, F.J. (1995) Biometry. Freeman, New York.
51. Stankowich, T. & Blumstein, D.T. (2005) Fear in animals: a meta-analysis and review of risk assessment. Proceedings of the Royal Society B: Biological Sciences, 272, 2627-2634.
52. Steffensen, J. (1989) Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiology and Biochemistry, 6, 49-59.
53. Verheyen, E., Blust, R. & Decleir, W. (1994) Metabolic rate, hypoxia tolerance and aquatic surface respiration of some lacustrine and riverine African cichlid fishes (Pisces: Cichlidae). Comparative Biochemistry and Physiology Part A: Physiology, 107, 403-411.
54. Watson, M., Aebischer, N.J. & Cresswell, W. (2007) Vigilance and fitness in grey partridges Perdix perdix: the effects of group size and foraging-vigilance trade-offs on predation mortality. Journal of Animal Ecology, 76, 211-221.
55. Yamamoto, T., Ueda, H. & Higashi, S. (1998) Correlation among dominance status, metabolic rate and otolith size in masu salmon. Journal of Fish Biology, 52, 281-290.
56. Zhang, J., Gilbert, D., Gooday, A.J., Levin, L., Naqvi, S.W.A., Middelburg, J.J., Scranton, M., Ekau, W., Peña, A., Dewitte, B., Oguz, T., Monteiro, P.M.S., Urban, E., Rabalais, N.N., Ittekkot, V., Kemp, W.M., Ulloa, O., Elmgren, R., Escobar-Briones, E. & Van Der Plas, A.K. (2010) Natural and human-induced hypoxia and consequences for coastal areas: synthesis and future development. Biogeosciences, 7, 1443-1467.