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Microgeographic variation in metabolic rate and energy storage of brown trout: countergradient selection or thermal sensitivity?

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Abstract

We examined the influence of habitat size, growth opportunity, and the thermal conditions experienced during early development on the standard metabolic rate (SMR) of juvenile brown trout (Salmo trutta) from six natural populations to contrast the hypothesis of countergradient selection in metabolic rate. The study populations differed significantly in SMR. Population means for SMR changed in response to the temperature experienced during the yolk-absorption stage, when the risk of oxygen deficit increases and the vulnerability to hypoxia is highest. We also found a strong negative correlation between the temperature experienced during the first 2 months after yolk resorption and SMR, which supports the hypothesis of countergradient variation. Moreover, we detected a strong negative correlation between an index of growth opportunity and relative lipid content, suggesting that the risk of energy shortfall could be a major force in the evolution of storage strategies. Our results suggest that temperature can shape the evolution of metabolic rate during the yolk-absorptive stage or the first feeding stage, while energy storage levels may be more sensitive to thermal constraints acting on growth rates.

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References

  • J.D. Allan (1995) Stream Ecology: Structure and Function of Running Waters Chapman and Hall NY

    Google Scholar 

  • D. Álvarez A.G. Nicieza (2005) ArticleTitleIs metabolic rate a reliable predictor of growth and survival of brown trout (Salmo trutta) in the wild? Can. J. Fish. Aquat. Sci. 62 643–649 Occurrence Handle10.1139/f04-223

    Article  Google Scholar 

  • M.P. Ayres J.M. Scriber (1994) ArticleTitleLocal adaptation to regional climates in Papilio canadensis (Lepidoptera: Papilionidae) Ecol. Monogr. 64 465–482 Occurrence Handle10.2307/2937146

    Article  Google Scholar 

  • J.M. Billerbeck E.T. Schultz D. Conover (2000) ArticleTitleAdaptive variation in energy acquisition and allocation among latitudinal populations of the Atlantic silverside Oecologia 122 210–219 Occurrence Handle10.1007/PL00008848

    Article  Google Scholar 

  • P. Calow (1977) ArticleTitleEcology, evolution and energetics: a study in metabolic adaptation Adv. Ecol. Res. 10 1–62 Occurrence Handle10.1016/S0065-2504(08)60233-0

    Article  Google Scholar 

  • A. Clarke (1993) ArticleTitleSeasonal acclimatization and latitudinal compensation in metabolism: do they exist? Funct. Ecol. 7 139–149 Occurrence Handle10.2307/2389880

    Article  Google Scholar 

  • D.O. Conover E.T. Schultz (1995) ArticleTitlePhenotypic similarity and the evolutionary significance of countergradient variation Trends Ecol. Evol. 10 248–252 Occurrence Handle10.1016/S0169-5347(00)89081-3

    Article  Google Scholar 

  • A.R. Cossins K. Bowler (1987) Temperature Biology of Animals Chapman and Hall NY

    Google Scholar 

  • W.D. Crill R.B. Huey G.W. Gilchrist (1996) ArticleTitleWithin- and between-generation effects of temperature on the morphology and physiology of Drosophila melanogaster Evolution 50 1205–1218 Occurrence Handle10.2307/2410661

    Article  Google Scholar 

  • C.J. Cutts C.E. Adams A. Campbell (2001) ArticleTitleStability of physiological and behavioural determinants of performance in Arctic char (Salvelinus alpinus) Can. J. Fish. Aquat. Sci. 58 961–968 Occurrence Handle10.1139/cjfas-58-5-961

    Article  Google Scholar 

  • M. Djawdan M.R. Rose T.J. Bradley (1997) ArticleTitleDoes selection for stress resistance lower metabolic rate? Ecology 78 828–837 Occurrence Handle10.2307/2266062

    Article  Google Scholar 

  • G.R. Dobush C.D. Ankney D.G. Krementz (1985) ArticleTitleThe effect of apparatus, extraction time, and solvent type on lipid extractions of snow geese Can. J. Zool. 63 1917–1920 Occurrence Handle1:CAS:528:DyaL2MXmtFSgtr4%3D

    CAS  Google Scholar 

  • A. Drud Jordan A. Jungersen J.F. Steffensen (2001) ArticleTitleOxygen consumption of East Siberian cod: no support for the metabolic cold adaptation theory J. Fish Biol. 59 818–823 Occurrence Handle10.1006/jfbi.2001.1692

    Article  Google Scholar 

  • J.M. Elliott (1972) ArticleTitleRates of gastric evaluation in brown trout, Salmo trutta L Fresh. Biol. 2 1–18 Occurrence Handle10.1111/j.1365-2427.1972.tb01575.x

    Article  Google Scholar 

  • J.M. Elliott (1994) Quantitative Ecology and the Brown Trout Oxford University Press Oxford

    Google Scholar 

  • J.M. Elliott M.A. Hurley J.A. Elliott (1997) ArticleTitleVariable effects of droughts on the density of a sea-trout Salmo trutta population over 30 years J. Appl. Ecol. 34 1229–1238 Occurrence Handle10.2307/2405234

    Article  Google Scholar 

  • A.P. Farrell (2002) ArticleTitleCardiorespiratory performance in salmonids during exercise at high temperature: insights into cardiovascular design limitations in fishes Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 132 797–810 Occurrence Handle12095864 Occurrence Handle1:STN:280:DC%2BD38zlt1CmsQ%3D%3D Occurrence Handle10.1016/S1095-6433(02)00049-1

    Article  PubMed  CAS  Google Scholar 

  • T. Garland SuffixJr. S.C. Adolph (1991) ArticleTitlePhysiological differentiation of vertebrate populations Ann. Rev. Ecol. Syst. 22 193–228 Occurrence Handle10.1146/annurev.es.22.110191.001205

    Article  Google Scholar 

  • L.G. Harshman A.A. Hoffmann A.G. Clark (1999) ArticleTitleSelection for starvation resistance in Drosophila melanogaster: physiological correlates, enzyme activities and multiple stress responses J. Evol. Biol. 12 370–379 Occurrence Handle1:CAS:528:DyaK1MXhvF2gsLg%3D Occurrence Handle10.1046/j.1420-9101.1999.00024.x

    Article  CAS  Google Scholar 

  • A.A. Hoffmann P.A. Parsons (1997) Extreme Environmental Change and Evolution Cambridge University Press Cambridge

    Google Scholar 

  • B.E. Huitema (1980) The Analysis of Covariance and Alternatives Wiley NY

    Google Scholar 

  • T.P. Hurst D.O. Conover (1998) ArticleTitleWinter mortality of young-of-the-year Hudson River striped bass (Morone saxatilis): size-dependent patterns and effects on recruitment Can. J. Fish. Aquat. Sci. 55 1122–1130 Occurrence Handle10.1139/cjfas-55-5-1122

    Article  Google Scholar 

  • M. Jasienski F.A. Bazzaz (1999) ArticleTitleThe fallacy of ratios and the testability of models in biology Oikos 84 321–326

    Google Scholar 

  • E. Kamler (1992) Early Life History of Fish: an Energetics Approach Chapman and Hall NY

    Google Scholar 

  • H.G. Kawall J.J. Torres B.D. Sidell G.N. Somero (2002) ArticleTitleMetabolic cold adaptation in Antarctic fishes: evidence from enzymatic activities of brain Mar. Biol. 140 279–286 Occurrence Handle10.1007/s002270100695

    Article  Google Scholar 

  • J.G. Kingsolver W.B. Watt (1983) ArticleTitleThermoregulatory strategies in Colias butterflies: thermal stress and the limits to adaptation in temporally varying environments Am. Nat. 121 32–55 Occurrence Handle10.1086/284038

    Article  Google Scholar 

  • A.T. Laugen A. Laurila K. Räsänen J. Merilä (2003) ArticleTitleLatitudinal countergradient variation in the common frog (Rana temporaria) developmental rates: evidence for local adaptation J.␣Evol. Biol. 16 1–10 Occurrence Handle10.1046/j.1420-9101.2003.00506.x

    Article  Google Scholar 

  • R. Levins (1969) ArticleTitleThermal acclimation and heat resistance in Drosophila species Am. Nat. 103 483–499 Occurrence Handle10.1086/282616

    Article  Google Scholar 

  • N.B. Metcalfe J.E. Thorpe (1990) ArticleTitleDeterminants of geographical variation in the age of seaward-migrating salmon, Salmo salar J. Anim. Ecol. 59 135–145 Occurrence Handle10.2307/5163

    Article  Google Scholar 

  • N.B. Metcalfe A.C. Taylor J.E. Thorpe (1995) ArticleTitleMetabolic rate, social status and life-history strategies in Atlantic salmon Anim. Behav. 49 431–436 Occurrence Handle10.1006/anbe.1995.0056

    Article  Google Scholar 

  • P. Mueller J. Diamond (2001) ArticleTitleMetabolic rate and environmental productivity: well-provisioned animals evolved to run and idle fast Proc. Nat. Acad. Sci. USA 98 12550–12554 Occurrence Handle11606744 Occurrence Handle1:CAS:528:DC%2BD3MXotFaitbk%3D Occurrence Handle10.1073/pnas.221456698

    Article  PubMed  CAS  Google Scholar 

  • A.G. Nicieza F. Braña M.M. Toledo (1991) ArticleTitleDevelopment of length-bimodality and smolting in wild stocks of Atlantic salmon, Salmo salar L., under different growth conditions J. Fish. Biol. 38 509–523 Occurrence Handle10.1111/j.1095-8649.1991.tb03138.x

    Article  Google Scholar 

  • A.G. Nicieza L. Reiriz F. Braña (1994) ArticleTitleVariation in digestive performance between geographically disjunct populations of Atlantic salmon: countergradient in passage time and digestion rate Oecologia 99 243–251 Occurrence Handle10.1007/BF00627736

    Article  Google Scholar 

  • K.I. O’Connor A.C. Taylor N.B. Metcalfe (2000) ArticleTitleThe stability of standard metabolic rate during a period of food deprivation in juvenile Atlantic salmon J. Fish Biol. 57 41–51 Occurrence Handle10.1111/j.1095-8649.2000.tb00774.x

    Article  Google Scholar 

  • A.F. Ojanguren F.G. Reyes-Gavilán F. Braña (2001) ArticleTitleThermal sensitivity of growth, food intake and activity of juvenile trout J. Therm. Biol. 26 165–170 Occurrence Handle11240221 Occurrence Handle10.1016/S0306-4565(00)00038-3

    Article  PubMed  Google Scholar 

  • G.C. Packard T.J. Boardman (1988) ArticleTitleThe misuse of ratios, indices, and percentages in ecophysiological research Physiol. Zool. 61 1–9

    Google Scholar 

  • R.H. Peters (1983) The Ecological Implications of Body Size Cambridge University Press Cambridge

    Google Scholar 

  • J.R. Post D.O. Evans (1989) ArticleTitleSize-dependent overwinter mortality of young-of-the-year yellow perch (Perca flavescens): laboratory, in situ enclosure, and field experiments Can. J. Fish. Aquat. Sci. 46 1958–1968

    Google Scholar 

  • J.R. Post E.A. Parkinson (2001) ArticleTitleEnergy allocation strategy in young fish: allometry and survival Ecology 82 1040–1051 Occurrence Handle10.2307/2679901

    Article  Google Scholar 

  • I.G. Priede (1985) Metabolic scope in fishes P. Tytler P. Calow (Eds) Fish Energetics: New Perspectives Croom Helm Kent, UK 33–63

    Google Scholar 

  • P.J. Rombough (1988) Respiratory gas exchange, aerobic metabolism, and effects of hypoxia during early life W.S. Hoar D.J. Randall (Eds) Fish Physiology NumberInSeriesXIA Academic Press NY 59–161

    Google Scholar 

  • E.T. Schultz D.O. Conover (1997) ArticleTitleLatitudinal differences in somatic energy storage: adaptive responses to seasonality in an estuarine fish (Atherinidae: Menidia menidia) Oecologia 109 516–529 Occurrence Handle10.1007/s004420050112

    Article  Google Scholar 

  • L.E. Siefert A.R. Carlson L.J. Herman (1974) ArticleTitleEffects of reduced oxygen concentrations on the early life stages of mountain whitefish, smallmouth bass, and white bass Progr. Fish-Cult. 36 186–190

    Google Scholar 

  • J.F. Steffensen (1989) ArticleTitleSome errors in respirometry of aquatic breathers: how to avoid and correct for them Fish. Physiol. Biochem. 6 49–59 Occurrence Handle10.1007/BF02995809

    Article  Google Scholar 

  • J.F. Steffensen (2002) ArticleTitleMetabolic cold adaptation of polar fish based on measurements of aerobic oxygen consumption: fact or artifact? Artifact! Comp. Biochem. Physiol. 132 789–795 Occurrence Handle10.1016/S1095-6433(02)00048-X

    Article  Google Scholar 

  • Å.V. Tåning (1952) ArticleTitleExperimental study of meristic characters in fishes Biol. Rev. Camb. Phil. Soc. 27 169–173

    Google Scholar 

  • J.-M. Vernier (1969) ArticleTitleTable chronologique du développement embryonarie de la truite arc-en-ciel, Salmo gairdneri Rich. 1836 Ann. d’Embryol. Morphog. 2 495–520

    Google Scholar 

  • T.M.L. Wigley (1985) ArticleTitleImpact of extreme events Nature 316 106–107

    Google Scholar 

  • D.E. Wohlschlag (1960) ArticleTitleMetabolism of an Antarctic fish and the phenomenon of cold adaptation Ecology 41 287–292 Occurrence Handle1:CAS:528:DyaF3MXltVaisg%3D%3D Occurrence Handle10.2307/1930217

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Ecology Unit, Department of Biology of Organisms and Systems, University of Oviedo, E-33006, Oviedo, Spain

    David Álvarez, José M. Cano & Alfredo G. Nicieza

  2. Department of Functional Biology, University of Oviedo, E-33006, Oviedo, Spain

    David Álvarez

  3. Department of Bio- and Environmental Sciences, Ecological Genetics Research Unit, University of Helsinki, FIN-00014, Helsinki, Finland

    José M. Cano & Alfredo G. Nicieza

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  1. David Álvarez
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  2. José M. Cano
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  3. Alfredo G. Nicieza
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Correspondence to Alfredo G. Nicieza.

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Co-ordinating editor: K. Lindtsröm

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Álvarez, D., Cano, J.M. & Nicieza, A.G. Microgeographic variation in metabolic rate and energy storage of brown trout: countergradient selection or thermal sensitivity?. Evol Ecol 20, 345–363 (2006). https://doi.org/10.1007/s10682-006-0004-1

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