Predator bioenergetics and the prey size spectrum: Do foraging costs determine fish production?

Journal of Theoretical Biology

Volumn 332, Issue , 2013, Pages 249-260

  Giacomini, Henrique C ^a   Shuter, Brian J ^a,b   Lester, Nigel P ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b ONTARIO MINISTRY OF NATURAL RESOURCES   (Canada)

Author keywords

Active metabolism; Body size; Functional response; Habitat dimensionality; Life history

Indexed keywords

BIOENERGETICS; BODY SIZE; FISH; FUNCTIONAL RESPONSE; INGESTION RATE; LIFE HISTORY; METABOLISM; NUMERICAL MODEL; PREDATOR; PREY SIZE;

ARTICLE; BIOENERGY; BODY SIZE; COMMUNITY STRUCTURE; CONTROLLED STUDY; FISH; FOOD WEB; FORAGING; LIFE HISTORY; MATHEMATICAL MODEL; METABOLISM; NONHUMAN; PREDATOR; PREDATOR PREY INTERACTION; PREY; PRIORITY JOURNAL; SATIETY; SWIMMING;

ACTIVE METABOLISM; BODY SIZE; FUNCTIONAL RESPONSE; HABITAT DIMENSIONALITY; LIFE HISTORY;

ANIMALS; ENERGY INTAKE; FISHES; FOOD CHAIN; MODELS, BIOLOGICAL; PREDATORY BEHAVIOR;

EID: 84880038057     PISSN: 00225193     EISSN: 10958541     Source Type: Journal    
DOI: 10.1016/j.jtbi.2013.05.004     Document Type: Article

References (111)

1. Abrams P.A. Foraging time optimization and interactions in food webs. Am. Nat. 1984, 124:80-96.
2. Abrams P. Life-history and the relationship between food availability and foraging effort. Ecology 1991, 72:1242-1252.
3. Abrams P.A., Ginzburg L.R. The nature of predation: prey dependent, ratio dependent or neither?. Trends in Ecology & Evolution 2000, 15:337-341.
4. Andersen K.H., Beyer J.E. Asymptotic size determines species abundance in the marine size spectrum. Am. Nat. 2006, 168:54-61.
5. Andersen K.H., Farnsworth K.D., Pedersen M., Gislason H., Beyer J.E. How community ecology links natural mortality, growth, and production of fish populations. ICES J. Mar. Sci. 2009, 66:1978-1984.
6. Aubin-Horth N., Gingras J., Boisclair D. Comparison of activity rates of 1+yellow perch (Perca flavescens) from populations of contrasting growth rates using underwater video observations. Can. J. Fish. Aquat. Sci. 1999, 56:1122-1132.
7. Benoit E., Rochet M.J. A continuous model of biomass size spectra governed by predation and the effects of fishing on them. J. Theor. Biol. 2004, 226:9-21.
8. Beverton R. Patterns of reproductive strategy parameters in some marine teleost fishes. J. Fish. Biol. 1992, 41:137-160.
9. Blackburn T., Gaston K. Animal body-size distributions - patterns, mechanisms and implications. Trends in Ecology & Evolution 1994, 9:471-474.
10. Blanchfield P.J., Tate L.S., Plumb J.M., Acolas M.-L., Beaty K.G. Seasonal habitat selection by lake trout (Salvelinus namaycush) in a small Canadian shield lake: constraints imposed by winter conditions. Aquatic Ecology 2009, 43:777-787.
11. Boisclair D., Leggett W. The importance of activity in bioenergetics models applied to actively foraging fishes. Can. J. Fish. Aquat. Sci. 1989, 46:1859-1867.
12. Boisclair D., Leggett W. Among-population variability of fish growth.1. Influence of the quantity of food consumed. Can. J. Fish. Aquat. Sci. 1989, 46:457-467.
13. Boisclair D., Leggett W. Among-population variability of fish growth.2. Influence of prey type. Can. J. Fish. Aquat. Sci. 1989, 46:468-482.
14. Boisclair D., Leggett W. Among-population variability of fish growth.3. Influence of fish community. Can. J. Fish. Aquatic Sci. 1989, 46:1539-1550.
15. Brose U. Body-mass constraints on foraging behavior determine population and food-web dynamics. Functional Ecology 2010, 24:28-34.
16. Brose U., Berlow E.L., Martinez N.D. From food webs to ecological networks: linking non-linear trophic interactions with nutrient competition. Dynamic Food Webs: Multispecies Assemblages, Ecosystem Development, and Environmental Change 2005, 27-36. Elsevier Academic Press, San Diego CA. P. De Ruiter, J.C. Moore, V. Wolters (Eds.).
17. Brose U., Jonsson T., Berlow E.L., Warren P., Banasek-Richter C., Bersier L.-F., Blanchard J.L., Brey T., Carpenter S.R., Blandenier M.-F.C., Cushing L., Dawah H.A., Dell T., Edwards F., Harper-Smith S., Jacob U., Ledger M.E., Martinez N.D., Memmott J., Mintenbeck K., Pinnegar J.K., Rall B.C., Rayner T.S., Reuman D.C., Ruess L., Ulrich W., Williams R.J., Woodward G., Cohen J.E. Consumer-resource body-size relationships in natural food webs. Ecology 2006, 87:2411-2417.
18. Brown J.H., Gillooly J.F. Ecological food webs: High-quality data facilitate theoretical unification. Proc. Natl. Acad. Sci. USA 2003, 100:1467-1468.
19. Brown J.H., Gillooly J.F., Allen A.P., Savage V.M., West G.B. Toward a metabolic theory of ecology. Ecology 2004, 85:1771-1789.
20. Chandrasekhar S. Stochastic problems in physics and astronomy. Rev. Mod. Phys. 1943, 15:1-89.
21. Charnov E.L. Life History Invariants: Some Explorations of Symmetry in Evolutionary Ecology 1993, Oxford University Press.
22. Charnov E.L., Turner T.F., Winemiller K.O. Reproductive constraints and the evolution of life histories with indeterminate growth. Proc. Natl. Acad. Sci. USA 2001, 98:9460-9464.
23. Clark P., Evans F. Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 1954, 35:445-453.
24. Clarke A., Johnston N.M. Scaling of metabolic rate with body mass and temperature in teleost fish. J. Anim. Ecol. 1999, 68:893-905.
25. Dabrowski K., Takashima F., Law Y. Bioenergetic model of planktivorous fish feeding, growth and metabolism - theoretical optimum swimming speed of fish larvae. J. Fish. Biol. 1988, 32:443-458.
26. Datta S., Delius G.W., Law R., Plank M.J. A stability analysis of the power-law steady state of marine size spectra. J. Math. Biol. 2011, 63:779-799.
27. Eby L., Rudstam L., Kitchell J. Predator responses to prey population-dynamics - an empirical-analysis based on lake trout growth-rates. Can. J. Fish. Aquat. Sci. 1995, 52:1564-1571.
28. Eklöf A., Jacob U., Kopp J., Bosch J., Castro-Urgal R., Chacoff N.P., Dalsgaard B., de Sassi C., Galetti M., Guimarães P.R., Lomáscolo S.B., González A.M.M., Pizo M.A., Rader R., Rodrigo A., Tylianakis J.M., Vázquez D.P., Allesina S. The dimensionality of ecological networks. Ecol. Lett. 2013, 10.1111/ele.12081.
29. Ernest S.K.M., Enquist B.J., Brown J.H., Charnov E.L., Gillooly J.F., Savage V., White E.P., Smith F.A., Hadly E.A., Haskell J.P., Lyons S.K., Maurer B.A., Niklas K.J., Tiffney B. Thermodynamic and metabolic effects on the scaling of production and population energy use. Ecol. Lett. 2003, 6:990-995.
30. Forseth T., Ugedal O., Jonsson B. The energy budget, niche shift, reproduction and growth in a population. J. Anim. Ecol. 1994, 63:116-126.
31. Giacomini H.C., DeAngelis D.L., Trexler J.C., Petrere M. Trait contributions to fish community assembly emerge from trophic interactions in an individual-based model. Ecol. Model. 2013, 251:32-43.
32. Gerritsen J. Size efficiency reconsidered - a general foraging model for free-swimming aquatic animals. Am. Nat. 1984, 123:450-467.
33. Griffiths D. Body size distributions in North American freshwater fish: large-scale factors. Global Ecol. Biogeogr. 2012, 21:383-392.
34. Haddon M. Modelling and Quantitative Methods in Fisheries 2011, Chapman and Hall, Boca Raton.
35. Hanson, P.C., Johnson, T.B., Schindler, D.E., Kitchell, J.K., 1997. Fish Bioenergetics 3.0. University of Wisconsin-Madison Center for Limnology and University of Wisconsin Sea Grant Institute.
36. Hartvig M., Andersen K.H., Beyer J.E. Food web framework for size-structured populations. J. Theor. Biol. 2011, 272:113-122.
37. Hastings A. Population Biology□: Concepts and Models 1997, Springer, New York.
38. Hastings, H.M., Sugihara, G., 1993. Fractals: a user's guide for the natural sciences.
39. Hayes D., Taylor W. Reproductive strategy in yellow perch (Perca flavescens) - effects of diet ontogeny, mortality, and survival costs. Can. J. Fish. Aquat. Sci. 1990, 47:921-927.
40. Heath D.D., Roff D.A. The role of trophic bottlenecks in stunting: A field test of an allocation model of growth and reproduction in yellow perch, Perca flavescens. Environ. Biol. Fishes 1996, 45:53-63.
41. Henderson B.A., Morgan G.E., Vaillancourt A. Growth, ingestion rates and metabolic activity of walleye in lakes with and without lake herring. J. Fish. Biol. 2004, 65:1270-1282.
42. Holling C.S. Some characteristics of simple types of predation and parasitism. Can. Entomol. 1959, 91:385-3998.
43. Holt R., Grover J., Tilman D. Simple rules for interspecific dominance in systems with exploitative and apparent competition. Am. Nat. 1994, 144:741-771.
44. Iles A.C., Rasmussen J.B. Indirect effects of metal contamination on energetics of yellow perch (Perca flavescens) resulting from food web simplification. Freshw. Biol. 2005, 50:976-992.
45. Janhunen M., Peuhkuri N., Piironen J. A comparison of growth patterns between a stunted and two large predatory Arctic charr populations under identical hatchery conditions. Environ. Biol. Fishes 2010, 87:113-121.
46. Jennings S., Blanchard J.L. Fish abundance with no fishing: predictions based on macroecological theory. J. Anim. Ecol. 2004, 73:632-642.
47. Jennings S., Mackinson S. Abundance-body mass relationships in size-structured food webs. Ecol. Lett. 2003, 6:971-974.
48. Jennings S., Pinnegar J.K., Polunin N.V.C., Boon T.W. Weak cross-species relationships between body size and trophic level belie powerful size-based trophic structuring in fish communities. J. Anim. Ecol. 2001, 70:934-944.
49. Jeschke J.M. When carnivores are "full and lazy". Oecologia 2007, 152:357-364.
50. Jeschke J.M., Kopp M., Tollrian R. Predator functional responses: Discriminating between handling and digesting prey. Ecol. Monogr. 2002, 72:95-112.
51. Jeschke J.M., Kopp M., Tollrian R. Consumer-food systems: why type I functional responses are exclusive to filter feeders. Biol. Rev. 2004, 79:337-349.
52. Jobling M. Fish Bioenergetics 1994, Springer.
53. Jonsson B., Skulason S., Snorrason S., Sandlund O., Malmquist H., Jonasson P., Gydemo R., Lindem T. Life-history variation of polymorphic arctic charr (Salvelinus alpinus). Can. J. Fish. Aquat. Sci. 1988, 45:1537-1547.
54. Juncos R., Milano D., Macchi P.J., Alonso M.F., Vigliano P.H. Response of rainbow trout to different food web structures in Northern Patagonia: implications for growth, bioenergetics, and invasiveness. Trans. Am. Fish. Soc. 2011, 140:415-428.
55. Kaufman S.D., Gunn J.M., Morgan G.E., Couture P. Muscle enzymes reveal walleye (Sander vitreus) are less active when larger prey (cisco, Coregonus artedi) are present. Can.J. Fish. Aquat. Sci. 2006, 63:970-979.
56. Kerr S. Simulation model of lake trout growth. J. Fish. Res. Board Can. 1971, 28:815.
57. Kerr S. Prey availability, metaphoetesis, and the size structures of lake trout stocks. Invest. Pesq. 1979, 43:187-198.
58. Kerr S., Ryder R. Niche theory and percid community structure. J. Fish. Res. Board Can. 1977, 34:1952-1958.
59. Knouft J.H., Page L.M. The evolution of body size in extant groups of North American freshwater fishes: speciation, size distributions, and Cope's rule. Am. Nat. 2003, 161:413-421.
60. Kooijman S.A.L.M. Dynamic Energy Budget Theory for Metabolic Organization 2010, Cambridge University Press, Cambridge, UK. 3rd edn.
61. Kozlowski J. Optimal allocation of resources explains interspecific life-history patterns in animals with indeterminate growth. Proc. R. Soc. Lon. Ser. B-Biol. Sci. 1996, 263:559-566.
62. Kozlowski J., Czarnoleski M., Danko M. Can optimal resource allocation models explain why ectotherms grow larger in cold?. Integr. Comp. Biol. 2004, 44:480-493.
63. Kozlowski J., Gawelczyk A.T. Why are species' body size distributions usually skewed to the right?. Functional Ecology 2002, 16:419-432.
64. Law R., Plank M.J., James A., Blanchard J.L. Size-spectra dynamics from stochastic predation and growth of individuals. Ecology 2009, 90:802-811.
65. Loeuille N., Loreau M. Evolutionary emergence of size-structured food webs. Proc. Natl. Acad. Sci. USA. 2005, 102:5761-5766.
66. Mackenzie B., Leggett W., Peters R. Estimating larval fish ingestion rates - can laboratory derived values be reliably extrapolated to the wild?. Mari. Ecol.-Prog. Ser. 1990, 67:209-225.
67. Matuszek J., Shuter B. Changes in lake trout growth and abundance after introduction of cisco into lake Opeongo, Ontario. Trans. Am. Fish. Soc. 1990, 119:718-729.
68. McCann K.S. Food Webs 2011, Princeton university Press.
69. Mittelbach G.G., Persson L. The ontogeny of piscivory and its ecological consequences. Can. J. Fish. Aquat.Sci. 1998, 55:1454-1465.
70. Munk P. Foraging behavior of larval cod (Gadus morhua) influenced by prey density and hunger. Mar. Biol. 1995, 122:205-212.
71. Naisbit R.E., Kehrli P., Rohr R.P., Bersier L-F. Phylogenetic signal in predator-prey body-size relationships. Ecology 2011, 92:2183-2189.
72. Oaten A., Murdoch W. Functional response and stability in predator-prey systems. Am. Nat. 1975, 109:289-298.
73. Ohlberger J., Staaks G., Hoelker F. Effects of temperature, swimming speed and body mass on standard and active metabolic rate in vendace (Coregonus albula). J. Comp. Physiol. B-Biochemical Systemic Environ. Physiol. 2007, 177:905-916.
74. Paloheimo J.E., Dickie L. Food and growth of fishes.3. Relations among food body size and growth efficiency. J. Fish. Res. Board Can. 1966, 23:1209.
75. Pawar S., Dell A.I., Savage V.M. Dimensionality of consumer search space drives trophic interaction strengths. Nature 2012, 10.1038/nature11131.
76. Pazzia I., Trudel M., Ridgway M., Rasmussen J.B. Influence of food web structure on the growth and bioenergetics of lake trout (Salvelinus namaycush). Can. J. Fish. Aquat. Sci. 2002, 59:1593-1605.
77. Perrin N., Sibly R., Nichols N. Optimal-growth strategies when mortality and production-rates are size-dependent. Evolutionary Ecology 1993, 7:576-592.
78. Persson L., Leonardsson K., de Roos A.M., Gyllenberg M., Christensen B. Ontogenetic scaling of foraging rates and the dynamics of a size-structured consumer-resource model. Theor. Popul. Biol. 1998, 54:270-293.
79. Petchey O.L., Beckerman A.P., Riede J.O., Warren P.H. Size, foraging, and food web structure. Proc. Natl. Acad. Sci. USA 2008, 105:4191-4196.
80. Peters R.H. The Ecological Implications of Body Size 1983, Cambridge University Press.
81. Plank, M.J., Law, R., 2011. Ecological drivers of stability and instability in marine ecosystems.
82. Pope J.G., Rice J.C., Daan N., Jennings S., Gislason H. Modelling an exploited marine fish community with 15 parameters - results from a simple size-based model. ICES J. Mar. Sci. 2006, 63:1029-1044.
83. Powell C.R., McKane A.J. Comparison of food webs constructed by evolution and by immigration. Ecological Complexity 2009, 6:316-327.
84. Quince C., Abrams P.A., Shuter B.J., Lester N.P. Biphasic growth in fish I: Theoretical foundations. J. Theor. Biol. 2008, 254:197-206.
85. Quince C., Shuter B.J., Abrams P.A., Lester N.P. Biphasic growth in fish II: Empirical assessment. J. Theor. Biol. 2008, 254:207-214.
86. Rennie M.D., Collins N.C., Shuter B.J., Rajotte J.W., Couture P. A comparison of methods for estimating activity costs of wild fish populations: more active fish observed to grow slower. Can. J. Fish. Aquat. Sci. 2005, 62:767-780.
87. Ricker W.E. Computation and Interpretation of Biological Statistics of Fish Populations, Bulletin of the Fisheries Research Board of Canada 1975, Department of the Environment Fisheries and Marine Service, Otawa.
88. Roff D.A. The Evolution of Life Histories: Theory and Analysis 1992, Springer.
89. Rosenzweig M., MacArthur R. Graphical representation and stability conditions of predator-prey interactions. Am. Nat. 1963, 97:209.
90. Saint-Jacques N., Harvey H.H., Jackson D.A. Selective foraging in the white sucker (Catostomus commersoni). Can. J. Zool.-Revue Canadienne De Zoologie 2000, 78:1320-1331.
91. Sherwood G.D., Kovecses J., Hontela A., Rasmussen J.B. Simplified food webs lead to energetic bottlenecks in polluted lakes. Can. J. Fish. Aquat. Sci. 2002, 59:1-5.
92. Sherwood G.D., Pazzia I., Moeser A., Hontela A., Rasmussen J.B. Shifting gears: enzymatic evidence for the energetic advantage of switching diet in wild-living fish. Can. J. Fish. Aquat. Sci. 2002, 59:229-241.
93. Sibly R.M., Grimm V., Martin B.J., Johnston A.S.A., Kułakowska K., Topping C.J., Calow P., Nabe-Nielsen J., Thorbek P., DeAngelis D.L. Representing the acquisition and use of energy by individuals in agent-based models of animal populations. Methods Ecology Evolution 2013, 4:151-161.
94. Steinhausen M.F., Steffensen J.F., Andersen N.G. Tail beat frequency as a predictor of swimming speed and oxygen consumption of saithe (Pollachius virens) and whiting (Merlangius merlangus) during forced swimming. Mar. Biol. 2005, 148:197-204.
95. Stewart D., Weininger D., Rottiers D., Edsall T. An energetics model for lake trout, Salvelinus namaycush - application. Canadian Journal of Fisheries and Aquatic Sciences 1983, 40:681-698.
96. Tang M., Boisclair D., Menard C., Downing J.A. Influence of body weight, swimming characteristics, and water temperature on the cost of swimming in brook trout (Salvelinus fontinalis). Canadian Journal of Fisheries and Aquatic Sciences 2000, 57:1482-1488.
97. Thygesen U., Farnsworth K., Andersen K., Beyer J. How optimal life history changes with the community size-spectrum. Proc. R. Soc. London B 2005, 272:1323-1331.
98. Troost T.A., Kooi B.W., Dieckmann U. Joint evolution of predator body size and prey-size preference. Evolutionary Ecology 2008, 22:771-799.
99. Trudel M., Tremblay A., Schetagne R., Rasmussen J.B. Estimating food consumption rates of fish using a mercury mass balance model. Can. J. Fish. Aquat. Sci. 2000, 57:414-428.
100. Trudel M., Tremblay A., Schetagne R., Rasmussen J.B. Why are dwarf fish so small? An energetic analysis of polymorphism in lake whitefish (Coregonus clupeaformis). Can. J. Fish. Aquat. Sci. 2001, 58:394-405.
101. Trudel M., Welch D.W. Modeling the oxygen consumption rates in Pacific salmon and steelhead: Model development. Trans. Am. Fish. Soc. 2005, 134:1542-1561.
102. Valdovinos F.S., et al. Consequences of adaptive behavior for the structure and dynamics of food webs. Ecol. Lett. 2010, 13:1546-1559.
103. Verhoef H.A., Morin P.J. Community Ecology Processes, Models, and Applications 2010, Oxford University Press.
104. Videler J., Nolet B. Costs of swimming measured at optimum speed - scale effects, differences between swimming styles, taxonomic groups and submerged and surface swimming. Comparative Biochemistry Physiol. A-Physiol. 1990, 97:91-99.
105. Videler J.J. Fish Swimming 1993, Chapman & Hall.
106. Ware D. Bioenergetics of pelagic fish - theoretical change in swimming speed and ration with body size. J. Fish. Res. Board Can. 1978, 35:220-228.
107. Weitz J.S., Levin S.A. Size and scaling of predator-prey dynamics. Ecol. Lett. 2006, 9:548-557.
108. Werner E., Gilliam J. The ontogenetic niche and species interactions in size structured populations. Annu. Rev. Ecol. Syst. 1984, 15:393-425.
109. Woodward G., Ebenman B., Emmerson M., Montoya J.M., Olesen J.M., Valido A., Warren P.H. Body size in ecological networks. Trends in Ecology & Evolution 2005, 20:402-409.
110. Ylikarjula J., Heino M., Dieckmann U. Ecology and adaptation of stunted growth in fish. Evolutionary Ecology 1999, 13:433-453.
111. Yodzis P., Innes S. Body size and consumer-resource dynamics. Am. Nat. 1992, 139:1151-1175.