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Adaptive responses of energy storage and fish life histories to climatic gradients. (English) Zbl 1411.92306
Summary: Energy storage is a common adaptation of fish living in seasonal environments. For some species, the energy accumulated during the growing season, and stored primarily as lipids, is crucial to preventing starvation mortality over winter. Thus, in order to understand the adaptive responses of fish life history to climate, it is important to determine how energy should be allocated to storage and how it trades off with the other body components that contribute to fitness. In this paper, we extend previous life history theory to include an explicit representation of how the seasonal allocation of energy to storage acts as a constraint on fish growth. We show that a strategy that privileges allocation to structural mass in the first part of the growing season and switches to storage allocation later on, as observed empirically in several fish species, is the strategy that maximizes growth efficiency and hence is expected to be favored by natural selection. Stochastic simulations within this theoretical framework demonstrate that the relative performance of this switching strategy is robust to a wide range of fluctuations in growing season length, and to moderate short-term (i.e., daily) fluctuations in energy intake and/or expenditure within the growing season. We then integrate this switching strategy with a biphasic growth modeling framework to predict typical growth rates of walleye Sander vitreus, a cool water species, and lake trout Salvelinus namaycush, a cold water specialist, across a climatic gradient in North America. As predicted, growth rates increased linearly with the duration of the growing season. Regression line intercepts were negative, indicating that growth can only occur when growing season length exceeds a threshold necessary to produce storage for winter survival. The model also reveals important differences between species, showing that observed growth rates of lake trout are systematically higher than those of walleye in relatively colder lakes. This systematic difference is consistent with both (i) the expected superior capacity of lake trout to withstand harsh winter conditions, and (ii) some degree of counter gradient adaptation of lake trout growth capacity to the climatic gradient covered by our data.
92D40 Ecology
92C15 Developmental biology, pattern formation
Full Text: DOI
[1] Abrams, P., Life-history and the relationship between food availability and foraging effort, Ecology, 72, 1242-1252, (1991)
[2] Abrams, P., Optimal traits when there are several costs - the interaction of mortality and energy costs in determining foraging behavior, Behav. Ecol., 4, 246-253, (1993)
[3] Abrams, P., Evolutionarily stable growth-rates in size-structured populations under size-related competition, Theor. Popul. Biol., 46, 78-95, (1994) · Zbl 0802.92024
[4] Abrams, P. A., Life-history strategies of optimal foragers, Theor. Popul. Biol., 24, 22-38, (1983) · Zbl 0528.92024
[5] Abrams, P. A., Can adaptive evolution or behaviour lead to diversification of traits determining a trade-off between foraging gain and predation risk?, Evol. Ecol. Res., 5, 653-670, (2003)
[6] Abrams, P. A.; Leimar, O.; Nylin, S.; Wiklund, C., The effect of flexible growth rates on optimal sizes and development times in a seasonal environment, Am. Nat., 147, 381-395, (1996)
[7] Angilletta, M., Thermal adaptation: A theoretical and empirical synthesis, (2009), Oxford University Press, New York
[8] Berg, O.; Finstad, A.; Solem, O.; Ugedal, O.; Forseth, T.; Niemela, E.; Arnekleiv, J.; Lohrmann, A.; Naesje, T., Pre-winter lipid stores in Young-of-year atlantic salmon along a north-south gradient, J. Fish Biol., 74, 1383-1393, (2009)
[9] Berg, O. K.; Rod, G.; Solem, O.; Finstad, A. G., Pre-winter lipid stores in Brown trout salmo trutta along altitudinal and latitudinal gradients, J. Fish Biol., 79, 1156-1166, (2011)
[10] Biro, P. A.; Morton, A. E.; Post, J. R.; Parkinson, E. A., Over-winter lipid depletion and mortality of age-0 rainbow trout (oncorhynchus mykiss), Can. J. Fish. Aquat. Sci., 61, 1513-1519, (2004)
[11] Biro, P. A.; Post, J. R.; Abrahams, M. V., Ontogeny of energy allocation reveals selective pressure promoting risk-taking behaviour in Young fish cohorts, Proc. R. Soc. B - Biol. Sci., 272, 1443-1448, (2005)
[12] Bonnet, X.; Bradshaw, D.; Shine, R., Capital vs. income breeding: an ectothermic perspective, Oikos, 83, 333-342, (1998)
[13] Bozek, M. A.; Baccante, D. A.; Lester, N. P., Walleye and sauger life history, (Barton, B. A., Biology, Management, and Culture of Walleye and Sauger, (2011), American Fisheries Society Bethesda, MD), 233-302
[14] Bradshaw, W. E.; Holzapfel, C. M., Evolution of animal photoperiodism, Ann. Rev. Ecol. Evol. Syst., 1-25, (2007)
[15] Bradshaw, W. E.; Holzapfel, C. M., Light, time, and the physiology of biotic response to rapid climate change in animals, Ann. Rev. Physiol., 147-166, (2010)
[16] Brown, J. H.; Gillooly, J. F.; Allen, A. P.; Savage, V. M.; West, G. B., Toward a metabolic theory of ecology, Ecology, 85, 1771-1789, (2004)
[17] Bull, C. D.; Metcalfe, N. B.; Mangel, M., Seasonal matching of foraging to anticipated energy requirements in anorexic juvenile salmon, Proc. R. Soc. B - Biol. Sci., 263, 13-18, (1996)
[18] Christie, G.; Regier, H., Measures of optimal thermal habitat and their relationship to yields for 4 commercial fish species, Can. J. Fish. Aquat. Sci., 45, 301-314, (1988)
[19] Clarke, A.; Johnston, N. M., Scaling of metabolic rate with body mass and temperature in teleost fish, J. Anim. Ecol., 68, 893-905, (1999)
[20] Conover, D.; Duffy, T.; Hice, L., The covariance between genetic and environmental influences across ecological gradients reassessing the evolutionary significance of countergradient and cogradient variation, Year Evol. Biol., 2009, 1168, 100-129, (2009)
[21] Day, T.; Abrams, P. A.; Chase, J. M., The role of size-specific predation in the evolution and diversification of prey life histories, Evolution, 56, 877-887, (2002)
[22] Dmitriew, C. M., The evolution of growth trajectories: what limits growth rate?, Biol. Rev., 86, 97-116, (2011)
[23] Emerson, K.; Bradshaw, W.; Holzapfel, C., Concordance of the Circadian clock with the environment is necessary to maximize fitness in natural populations, Evolution, 62, 979-983, (2008)
[24] Enberg, K.; Jørgensen, C.; Dunlop, E. S.; Varpe, Ø.; Boukal, D. S.; Baulier, L.; Eliassen, S.; Heino, M., Fishing-induced evolution of growth: concepts, mechanisms, and the empirical evidence, Mar. Ecol., 33, 1-25, (2012)
[25] 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., 6, 990-995, (2003)
[26] Finstad, A. G.; Berg, O. K.; Forseth, T.; Ugedal, O.; Naesje, T. F., Adaptive winter survival strategies: defended energy levels in juvenile atlantic salmon along a latitudinal gradient, Proc. R. Soc. B - Biol. Sci., 277, 1113-1120, (2010)
[27] Froese, R.; Pauly, D., Fishbase, (2012), World Wide Web electronic Publication, 〈www.fishbase.org〉 (accessed January 2012)
[28] Hasnain, S. B.J.; Shuter; Minns, C. K., Phylogeny influences the relationships linking key ecological thermal metrics for north American freshwater fish species, Can. J. Fish. Aquat. Sci, 70, 964-972, (2013)
[29] Henderson, B. A.; Wong, J. L.; Nepszy, S. J., Reproduction of walleye in lake erie: allocation of energy, Can. J. Fish. Aquat. Sci, 53, 127-133, (1996)
[30] Hurst, T. P.; Conover, D. O., Seasonal and interannual variation in the allometry of energy allocation in juvenile striped bass, Ecology, 84, 3360-3369, (2003)
[31] IPCC, I.P. on C.C., 2005. IPCC Data Distribution Centre: Global 30-Year Means.
[32] Kooijman, S. A.L. M.; Troost, T. A., Quantitative steps in the evolution of metabolic organisation as specified by the dynamic energy budget theory, Biol. Rev., 82, 113-142, (2007)
[33] Kooijman, S. A.L. M., Dynamic energy and mass budgets in biological systems, (2000), Cambridge University Press Cambridge, United Kingdon
[34] Kozlowski, J., Optimal allocation of resources explains interspecific life-history patterns in animals with indeterminate growth, Proc. R. Soc. B - Biol. Sci., 263, 559-566, (1996)
[35] Kozlowski, J.; Teriokhin, A., Allocation of energy between growth and reproduction: the Pontryagin maximum principle solution for the case of age- and season-dependent mortality, Evol. Ecol. Res., 1, 423-441, (1999)
[36] Legendre, L., Legendre, P., 1998. Numerical Ecology, second ed. Elsevier Science Publishers, Amsterdam. · Zbl 1033.92036
[37] Lester, N. P.; Shuter, B. J.; Abrams, P. A., Interpreting the von bertalanffy model of somatic growth in fishes: the cost of reproduction, Proc. R. Soc. London B, 271, 1625-1631, (2004)
[38] Lee, W.-S.; Monaghan, P.; Metcalfe, N. B., Experimental demonstration of the growth rate-lifespan trade-off, Proc. R. Soc. B - Biol. Sci., 280, 20122370, (2012)
[39] Lima, S.; Dill, L., Behavioral decisions made under the risk of predation - a review and prospectus, Can. J. Zool., 68, 619-640, (1990)
[40] McDermid, J. L.; Shuter, B. J.; Lester, N. P., Life history differences parallel environmental differences among north American lake trout (salvelinus namaycush) populations, Can. J. Fish. Aquat. Sci., 67, 314-325, (2010)
[41] Mogensen, S.; Post, J. R., Energy allocation strategy modifies growth-survival trade-offs in juvenile fish across ecological and environmental gradients, Oecologia, 168, 923-933, (2012)
[42] Nelissen, M., Does body size affect the ranking of a cichlid fish in a dominance hierarchy?, J. Ethol., 10, 153-156, (1992)
[43] Nisbet, R. M.; Muller, E. B.; Lika, K.; Kooijman, S. A.L. M., From molecules to ecosystems through dynamic energy budget models, J. Anim. Ecol., 69, 913-926, (2000)
[44] Nisbet, R. M.; Jusup, M.; Klanjscek, T.; Pecquerie, L., Integrating dynamic energy budget (DEB) theory with traditional bioenergetic models, J. Exp. Biol., 215, 892-902, (2012)
[45] Pauly, D., On the interrelationships between natural mortality, growth-parameters, and mean environmental-temperature in 175 fish stocks, J. Du Cons., 39, 175-192, (1980)
[46] Persson, L.; Andersson, J.; Wahlstrom, E.; Eklov, P., Size-specific interactions in lake systems: predator gape limitation and prey growth rate and mortality, Ecology, 77, 900-911, (1996)
[47] 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., 63, 1029-1044, (2006)
[48] Pörtner, H., Climate-dependent evolution of antarctic ectotherms: an integrative analysis, Deep-Sea Res. II, 53, 1071-1104, (2006)
[49] Post, J. R.; Parkinson, E. A., Energy allocation strategy in Young fish: allometry and survival, Ecology, 82, 1040-1051, (2001)
[50] Quince, C.; Abrams, P. A.; Shuter, B. J.; Lester, N. P., Biphasic growth in fish I: theoretical foundations, J. Theor. Biol., 254, 197-206, (2008) · Zbl 1400.92063
[51] Quince, C.; Shuter, B. J.; Abrams, P. A.; Lester, N. P., Biphasic growth in fish II: empirical assessment, J. Theor. Biol., 254, 207-214, (2008) · Zbl 1400.92064
[52] Roff, D. A., Life History Evolution, (2002), Sinauer Associates Sunderland, MA
[53] Schultz, E. T.; Conover, D. O., Latitudinal differences in somatic energy storage: adaptive responses to seasonality in an estuarine fish (atherinidae: menidiamenidia), Oecologia, 109, 516-529, (1997)
[54] Shul’man, G. E., Life cycles of fish, (1974), John Wiley and Sons New York
[55] Shulman, G. E.; Love, R. M., The biochemical ecology of marine fishes, (1999), Academic Press, London
[56] Shuter, B.; Schlesinger, D.; Zimmerman, A., Empirical predictors of annual surface-water temperature cycles in north American lakes, Can. J. Fish. Aquat. Sci., 40, 1838-1845, (1983)
[57] Shuter, B. J.; Finstad, A. G.; Helland, I. P.; Zweimueller, I.; Hoelker, F., The role of winter phenology in shaping the ecology of freshwater fish and their sensitivities to climate change, Aquat. Sci., 74, 637-657, (2012)
[58] Shuter, B. J.; Lester, N.; LaRose, J.; Purchase, C.; Vascotto, K.; Morgan, G.; Collins, N.; Abrams, P., Optimal life histories and food web position: linkages among somatic growth, reproductive investment, and mortality, Can. J. Fish. Aquat. Sci., 62, 738-746, (2005)
[59] Stewart, D.; Weininger, D.; Rottiers, D.; Edsall, T., An energetics model for lake trout, salvelinus namaycush - application, Can. J. Fish. Aquat. Sci., 40, 681-698, (1983)
[60] Varpe, Ø.; Jørgensen, C.; Tarling, G. A.; Fiksen, Ø., The adaptive value of energy storage and capital breeding in seasonal environments, Oikos, 118, 363-370, (2009)
[61] Werner, E.; Gilliam, J., The ontogenetic niche and species interactions in size structured populations, Ann. Rev. Ecol. Syst., 15, 393-425, (1984)
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