Adaptive trade-offs in juvenile salmonid metabolism associated with habitat partitioning between coho salmon and steelhead trout in coastal streams

Journal of Animal Ecology

Volumn 80, Issue 5, 2011, Pages 1012-1023

  Van Leeuwen, Travis E ^a   Rosenfeld, Jordan S ^a   Richards, Jeffrey G ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Adaptive trade offs; Food ration; Habitat partitioning; Hatchery vs. wild; Life history; Oncorhynchus kisutch; Oncorhynchus mykiss; Salmonid growth

Indexed keywords

ANTIPREDATOR DEFENSE; COASTAL ZONE; COEXISTENCE; DIVERGENCE; ECOPHYSIOLOGY; ENVIRONMENTAL GRADIENT; FOOD CONSUMPTION; GROWTH RATE; HABITAT FRAGMENTATION; HABITAT USE; HATCHERY; JUVENILE; LIFE HISTORY TRAIT; METABOLISM; MIGRATORY BEHAVIOR; NICHE PARTITIONING; RESOURCE ALLOCATION; SALMONID; STREAM; SURVIVAL; TRADE-OFF; WILD POPULATION;

ADAPTATION; ANIMAL; ARTICLE; CANADA; COMPARATIVE STUDY; EATING; ECOSYSTEM; ENERGY METABOLISM; FOOD INDUSTRY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ONCORHYNCHUS KISUTCH; OXYGEN CONSUMPTION; PHYSIOLOGY; RAINBOW TROUT; RIVER; SWIMMING; WILD ANIMAL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, WILD; BRITISH COLUMBIA; EATING; ECOSYSTEM; ENERGY METABOLISM; FISHERIES; ONCORHYNCHUS KISUTCH; ONCORHYNCHUS MYKISS; OXYGEN CONSUMPTION; RIVERS; SWIMMING;

ONCORHYNCHUS KISUTCH; ONCORHYNCHUS MYKISS; SALMO SALAR; SALMONIDAE; SALVELINUS FONTINALIS; VERTEBRATA;

EID: 79960839410     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/j.1365-2656.2011.01841.x     Document Type: Article

References (87)

1. Alsop, D.H. & Wood, C.M. (1997) The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout (Oncorhynchus mykiss). The Journal of Experimental Biology, 200, 2337-2346.
2. Alvarez, D., Cano, J.M. & Nicieza, A.G. (2006) Microgeographic variation in metabolic rate and energy storage of brown trout: countergradient selection or thermal sensitivity? Evolutionary Ecology, 20, 345-363.
3. Alvarez, D. & Metcalfe, N.B. (2007) The tradeoff between catch-up growth and escape speed: variation between habitats in the cost of compensation. Oikos, 116, 1144-1151.
4. Alvarez, 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.
5. Arendt, J.D. (1997) Adaptive intrinsic growth rates: an integration across taxa. Quarterly Review of Biology, 72, 149-177.
6. Arendt, J.D. & Wilson, D.S. (1997) Optimistic growth: competition and an ontogenetic niche-shift select for rapid growth in pumpkinseed sunfish (Lepomis gibbosus). Evolution, 51, 1946-1954.
7. Bams, R.A. (1967) Differences in performance of naturally and artificially propagated sockeye salmon migrant fry, as measured with swimming and predation tests. Journal of the Fisheries Research Board of Canada, 24, 1117-1153.
8. Billerbeck Jr, J.M., Lankford Jr, T.E. & Conover, D.O. (2001) Evolution of intrisic growth and energy acquisition rates. I. Trade-offs with swimming performance in Menidia menidia. Evolution, 55, 1863-1872.
9. Biro, P.A. & Stamps, J.A. (2008) Are animal personality traits linked to life-history productivity? Trends in Ecology & Evolution, 23, 361-368.
10. 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.
11. Bisson, P.A., Sullivan, K. & Nielsen, J.L. (1988) Channel hydraulics, habitat use, and body form of juvenile coho salmon, steelhead and cutthroat trout in streams. Transactions of the American Fisheries Society, 117, 262-273.
12. Bochdansky, A.B., Gronkjaer, P., Herra, T.P. & Leggett, W.C. (2005) Experimental evidence for selection fish larvae with high metabolic rates in a food limited environment. Marine Biology, 147, 1413-1417.
13. Boily, P. (2002) Individual variation in metabolic traits of wild nine-banded armadillos (Dasypus novemcinlus), and the aerobic capacity model for the evolution of endothermy. Journal of Experimental Biology, 205, 3207-3214.
14. Booth, D.J. (1990) Effect of water temperature on stomach evacuation rates and estimates of daily food intake of bluegill sunfish (Lepomis macrochirus Rafinesque). Canadian Journal of Zoology, 68, 591-595.
15. Bozinovic, S., Rojas, J.M., Broitman, B.R. & Vasquez, R.A. (2009) Basal metabolism is correlated with habitat productivity among populations of degus (Octodon degus). Comparative Biochemistry and Physiology Part A, 152, 560-564.
16. Brett, J.R. (1964) The respiratory metabolism and swimming performance of young sockeye salmon. Journal of the Fisheries Research Board of Canada, 21, 1183-1226.
17. Brett, J.R. (1971) Satiation time, appetite and maximum food intake of Sockeye salmon (Oncorhynchus nerka). Journal of the Fisheries Research Board of Canada, 28, 409-415.
18. Brett, J.R., Hollands, H. & Alerdice, D.F. (1958) The effect of temperature on the cruising speed of young sockeye and coho salmon. Journal of the Fisheries Research Board of Canada, 15, 587-605.
19. Bugert, R.M. & Bjornn, T.C. (1991) Habitat use by steelhead and coho salmon and their responses to predators and cover in laboratory streams. Transaction of the American Fisheries Society, 120, 486-493.
20. Cano, J.M. & Nicieza, A.G. (2006) Temperature, metabolic rate, and constraints on locomotor performance in ectotherm vertebrates. Functional Ecology, 20, 464-470.
21. Careau, V., Reale, D., Humphries, M.M. & Thomas, D. (2010) The pace of life under artificial selection: personality, energy expenditure, and longevity are correlated in domestic dogs. American Naturalist, 175, 753-758.
22. Chiba, S., Arnott, S.A. & Conover, D.O. (2007) Coevolution of foraging behavior with intrinsic growth rate: risk taking in naturally and artificially selected growth genotypes of Menidia menidia. Oecologia, 15, 237-246.
23. Conover, D.O. & Present, T.C. (1990) Countergradient variation in growth rate: compensation for length of the growing season among Atlantic silversides from different latitudes. Oecologia (Berlin), 83, 316-324.
24. Cutts, C.J., Metcalfe, N.B. & Taylor, A.C. (2002) Juvenile Atlantic Salmon (Salmo salar) with relatively high standard metabolic rates have small metabolic scopes. Functional Ecology, 16, 73-78.
25. Djawadan, M., Rose, M.R. & Bradley, T.J. (1997) Does selection for stress resistance lower metabolic rates? Ecology, 78, 828-837.
26. Ege, R. & Krough, A. (1914) On the relation between the temperature and the respiratory exchange in fishes. International Review of Hydrobiology Hydrograph, 7, 48-55.
27. Fangue, N.A., Mandic, M., Richards, J.G. & Schulte, P.M. (2008) Swimming performance and energetics as a function of temperature in Killifish Fundulus heteroclitus. Physiological and Biochemical Zoology, 81, 389-401.
28. 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.
29. Finstad, A.G., Forseth, T., Jonsson, B., Bellier, E., Hesthagen, T., Jensen, A.J., Hessen, D.O. & Foldvik, A. (2011) Competition exclusion along climate gradients: energy efficiency influences the distribution of two salmonid fishes. Global Change Biology, 17, 1703-1711.
30. Fleming, I.A., Agustsson, T., Finstad, B., Johnsson, J.I. & Bjornsson, B.T. (2002) Effects of domestication on growth physiology and endocrinology of Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences, 59, 1323-1330.
31. Forseth, T., Naesje, T.F., Jonsson, B. & Harsaker, K. (1999) Juvenile migration in brown trout: a consequence of energetic state. Journal of Animal Ecology, 68, 783-793.
32. Fraser, F.J. (1969) Population density effects on survival and growth of juvenile coho salmon and steelhead trout in experimental stream channels. Symposium on Salmon and Trout in Stream (ed. T.G. Northcote), pp. 253-266. University of British Columbia Press, Vancouver, BC.
33. Garland Jr, T. & Adolph, S.C. (1991) Physiological differentiation of vertebrate populations. Annual Review of Ecology and Systematics, 22, 193-228.
34. van Gils, J.A., Dekinga, A., van den Hout, P.J., Spaans, B. & Piersma, T. (2007) Digestive organ size and behavior of red knots (Calidris canutus) indicate the quality of their benthic food stocks. Israel Journal of Ecology and Evolution, 53, 329-346.
35. Gross, M.R. (1998) One species with two biologies: Atlantic salmon (Salmo salar) in the wild and in aquaculture. Canadian Journal of Fisheries and Aquatic Sciences, 55(Suppl. 1), 131-144.
36. Hart, P.J.B. & Gill, A.B. (1992) Constraints on prey size selection by the three-spined stickleback: energy requirements and the capacity of fullness of the gut. Journal of Fish Biology, 40, 205-218.
37. Hartmann, G.F. (1965) The role of behavior in the ecology and interaction of underyearling coho salmon (Oncorhynchus kisutch) and steelhead trout (Salmo gairdneri). Journal of Fisheries Research Board of Canada, 22, 1035-1081.
38. Hayes, J.W., Stark, J.D. & Shearer, K.A. (2000) Development and test of a whole-lifetime foraging and bioenergetics growth model for drift-feeding brown trout. Transactions of the American Fisheries Society, 129, 315-332.
39. Hume, I.D. (1989) Optimal digestive strategies in mammalian herbivores. Physiological Zoology, 62, 1145-1163.
40. Jain, K.E., Birtwell, I.K. & Farrell, A.P. (1998) Repeat swimming performance of mature sockeye salmon following a brief recovery period: a proposed measure of fish health and water quality. Canadian Journal of Zoology, 76, 1488-1498.
41. Jobling, M. (1981) The influences of feeding on the metabolic rate of fishes: a short review. Journal of Fish Biology, 18, 385-400.
42. Johnston, J.M. (1970) Food and Feeding Habits of juvenile Coho Salmon and Steelhead Trout in Worthy Creek. MSc Thesis. University of Washington, Seattle, WA.
43. Killen, S.S., Costa, I., Brown, J.A. & Gamperl, K.A. (2007) Little left in the tank: metabolic scaling in marine teleosts and its implications for aerobic scope. Proceedings of the Royal Society B, 274, 431-438.
44. Kleiber, M. (1961) The Fire of Life: An Introduction to Animal Energetics. John Wiley and Sons, New York, London.
45. Kolok, A.S. (1991) Photoperiod alters the critical swimming speed of juvenile largemouth bass, Micropterus salmoides, acclimated to cold water. Copeia, 1991, 1085-1090.
46. Lankford, T.E., Billerbeck Jr, J.M. & Conover, D.O. (2001) Evolution of intrisic growth and energy acquisition rates. II. Trade-offs with vulnerability to predation in Menidia menidia. Evolution, 55, 1873-1881.
47. Larivee, M.L., Boutin, S., Speakman, J.R., McAdam, A.G. & Humphries, M.M. (2010) Associations between over-winter survival and resting metabolic rate in juvenile North American red squirrels. Functional Ecology, 24, 597-607.
48. Lee, C.G., Farrell, A.P., Lotto, A., MacNutt, M.J., Hinch, S.G. & Healey, M.C. (2003) The effect of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. kisutch) salmon stocks. The Journal of Experimental Biology, 206, 3239-3251.
49. Lovegrove, B.G. (2003) The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. Journal of Comparative Physiology B, 173, 87-112.
50. Mathot, K.J., Godde, S., Careau, V., Thomas, D.W. & Giraldeau, L. (2009) Testing dynamic variance-sensitive foraging using individual differences in basal metabolic rates of zebra finches. Oikos, 118, 545-552.
51. 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.
52. 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.
53. Millidine, K.J., Armstrong, J.D. & Metcalfe, N.B. (2009) Juvenile salmon with high standard metabolic rates have higher energy cost but can process meals faster. Proceedings of the Royal Society B, 276, 2103-2108.
54. Milton, K. (1981) Food choice and digestive strategies of two sympatric primate species. The American Naturalist, 117, 496-505.
55. Molenaar, D., van Berlo, R., de Ridder, D. & Teusink, B. (2009) Shifts in growth strategies reflect tradeoffs in cellular economics. Molecular Systems Biology, 5, 323.
56. Morinville, G.R. & Rasmussen, J.B. (2003) Early juvenile bioenergetic differences between anadromous and resident brook trout (Salvelinus fontinalis). Canadian Journal of Aquatic Science, 60, 401-410.
57. Morinville, G.R. & Rasmussen, J.B. (2008) Distinguishing between juvenile anadromous and resident brook trout (Salvelinus fontinalis) using morphology. Environmental Biology of Fishes, 81, 171-184.
58. Mueller, P. & Diamond, J. (2001) Metabolic rate and environmental productivity: well provisioned animals evolved to run and idle fast. Proceedings of the National Academy of Sciences of the United States of America, 89, 12550-12554.
59. Nicieza, N.A., Reiriz, L. & Brana, F. (1994) Variation in digestive performance between geographically disjunct populations of Atlantic salmon: countergradient in passage time and digestion rate. Oecologia, 99, 243-251.
60. Nislow, K.H., Folt, C.L. & Parrish, D.L. (1999) Favorable foraging locations for young Atlantic salmon: application to habitat and population restoration. Ecological Applications, 9, 1085-1099.
61. Petersson, E., Jarvi, T., Steffner, N.G. & Ragnarsson, B. (1996) The effect of domestication on some life history traits of sea trout and Atlantic salmon. Journal of Fish Biology, 48, 776-791.
62. Plaut, I. (2001) Critical swimming speed: its ecological relevance. Comparative Biochemistry and Physiology, 131, 41-50.
63. Post, J.R. & Evans, D.O. (1989) Size dependent over-winter mortality of young-of-the-year yellow perch (Perca flavescens): laboratory, in situ enclosure, and field experiments. Canadian Journal of Fisheries and Aquatic Sciences, 46, 1958-1968.
64. Post, J.R. & Parkinson, E.A. (2001) Energy allocation strategy in young fish: allometry and survival. Ecology, 82, 1040-1051.
65. Puckett, K.J. & Dill, L.M. (1985) The energetics of feeding territoriality in juvenile coho salmon (Oncorhynchus kisutch). Behaviour, 92, 97-111.
66. Quinn, T.P. & Peterson, N.P. (1996) The influence of habitat complexity and fish size on overwintering survival and growth of individually marked juvenile coho salmon (Oncorhynchus kisutch) in Big Beef Creek, Washington. Canadian Journal of Fisheries and Aquatic Sciences, 53, 1555-1564.
67. Ricker, W.E. (1975) Computation and interpretation of biological statistics of fish populations. Bulletin of the Fisheries Research Board of Canada, 191.
68. Ridgway, M.S. (2008) A roadmap for coasters: landscapes, life histories, and the conservation of brook trout. Transactions of the American Fisheries Society, 137, 1179-1191.
69. Robinson, B.W. & Wilson, D.S. (1994) Character release and displacement in fishes: a neglected literature. The American Naturalist, 144, 596-627.
70. Schluter, D. (1993) Adaptive radiation in sticklebacks: size, shape, and habitat use efficiency. Ecology, 74, 699-709.
71. Schluter, D. (1995) Adaptive radiation in sticklebacks: trade-offs in breeding performance and growth. Ecology, 76, 82-90.
72. Schultz, E.T. & Conover, D.O. (1997) Latitudinal differences in somatic energy storage: adaptive responses to seasonality in an estuarine fish (Atherinidae: Menidia menidia). Oecologia, 109, 516-529.
73. Shuter, B.J. & Post, J.R. (1990) Climate, population viability, and the zoogeography of temperate fishes. Transactions of the American Fisheries Society, 119, 314-336.
74. Sibly, R.M. (1981) Strategies of digestion and defecation. Physiological Ecology: An Evolutionary Approach to Resource Use (eds C.R. Townsend & P. Calow), pp. 109-139. Blackwell, Oxford.
75. Speakman, J.R., Krol, E. & Johnson, M.S. (2004) The functional significance of individual variation in basal metabolic rate. Physiological and Biochemical Zoology, 77, 900-915.
76. Steffensen, J.F. (1989) Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiology and Biochemistry, 6, 49-59.
77. Stevens, D.E. (1992) Use of plastics materials in oxygen-measuring systems. Journal of Applied Physiology, 72, 801-804.
78. Steyermark, A.C. (2002) A high standard metabolic rate constrains growth. Zoology, 105, 147-151.
79. Sullivan, K., Martin, D.J., Cardwell, R.D., Toll, J.E. & Duke, S. (2001) An Analysis of the Effects of Temperature on Salmonids of the Pacific Northwest with Implications for Selecting Temperature Criteria. Sustainable Ecosystems Institute, Portland, OR.
80. Sundstrom, F.L., Lohmus, M. & Devlin, R.H. (2005) Selection on increased intrinsic growth rates in coho salmon, Oncorhynchus kisutch. Evolution, 59, 1560-1569.
81. Taylor, E.B. & McPhail, J.D. (1985) Variation in body morphology among British Columbia populations of coho salmon, Oncorhynchus kisutch. Canadian Journal of Fisheries and Aquatic Sciences, 42, 2020-2028.
82. Tucker, S. & Rasmussen, J.B. (1999) Using 137Cs to measure and compare bioenergetic budgets of juvenile Atlantic salmon (Salmo salar) and brook trout (Salvelinus fontinalis) in the field. Canadian Journal of Fisheries and Aquatic Sciences, 56, 875-887.
83. Van Leeuwen, T.E. (2010) Variation in Metabolic Rate Between Individuals and Species: Cryptic Physiological Tradeoffs Underlying Habitat Partitioning and Life History Strategies of Juvenile Salmonids. MSc Thesis. University of British Columbia, Canada.
84. Wieser, W. (1985) Developmental and metabolic constraints of the scope for activity in young rainbow trout (Salmo gairdneri). Journal of Experimental Biology, 118, 133-142.
85. Wurtsbaugh, W.A. & Davis, G.E. (1977) Effects of temperature and ration level on the growth and food conversion efficiency of Salmo gairdneri, Richardson. Journal of Fish Biology, 11, 87-98.
86. Young, K.A. (2001) The Effects of Size Asymmetries and Habitat Diversity on Interspecific Interactions in Juvenile Salmonids (Oncorhynchus sp.). PhD Thesis. University of British Columbia, Canada.
87. Young, K.A. (2004) Asymmetric competition habitat selection, and niche overlap in juvenile salmonids. Ecology, 85, 134-149.