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Effects of temperature on specific dynamic action in Atlantic cod Gadus morhua

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Abstract

Growth requires that energy is directed towards ingestion, digestion, absorption and assimilation of a meal; energy expenditures are often expressed as the specific dynamic action (SDA). While SDA is an important part of fish energy budgets and strongly affected by water temperature, temperature effects are not known across a wide temperature range in Atlantic cod Gadus morhua. The objective of this study was to examine effects of temperature (2, 5, 10, 15 or 20 °C) on the energetic cost and time used for SDA in juvenile G. morhua by intermittent flow respirometry. At each temperature, G. morhua were fed a meal of herring (Clupea harengus) corresponding to 5 % of the body mass. Standard metabolic rates measured pre-feeding and post-feeding metabolic rates were measured to determine SDA. The study showed that SDA coefficients (%, SDA energy divided by meal energy) were significantly lower at 2 and 10 °C (5.4–6.3 %) compared to 5, 15 and 20 °C (10.4–12.4 %), while SDA duration increased significantly from 80 h at 10 °C to 130–160 h at 2, 15 and 20 °C and reached a maximum of 250 h at 5 °C. The significant decrease in SDA duration at 10 °C combined with a low SDA coefficient suggests that water temperatures close to 10 °C may represent the optimum temperatures for SDA in this population of G. morhua. Our results suggest that SDA is not a simple function of temperature, but may vary with temperature in a more complex fashion.

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References

  • Andersen NG (2012) Influences of potential predictor variables on gastric evacuation in Atlantic cod Gadus morhua feeding on fish prey: parameterization of a generic model. J Fish Biol 80(3):595–612. doi:10.1111/j.1095-8649.2011.03195.x

    Article  CAS  PubMed  Google Scholar 

  • Behrens JW, Axelsson M, Neuenfeldt S, Seth H (2012) Effects of hypoxic exposure during feeding on SDA and postprandial cardiovascular physiology in the Atlantic cod, Gadus morhua. PLoS One 7(9):e46227. doi:10.1371/journal.pone.0046227

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bjornsson B, Steinarsson A, Oddgeirsson M (2001) Optimal temperature for growth and feed conversion of immature cod (Gadus morhua L.). ICES J Mar Sci 58(1):29–38. doi:10.1006/jmsc.2000.0986

    Article  Google Scholar 

  • Brown CR, Cameron JN (1991) The relationship between specific dynamic action (SDA) and protein-synthesis rates in the channel catfish. Physiol Zool 64(1):298–309

    CAS  Google Scholar 

  • Bureau DP, Kaushik SJ, Cho CY (2002) Bioenergetics. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, London, pp 1–59

    Google Scholar 

  • Capossela K, Brill R, Fabrizio M, Bushnell P (2012) Metabolic and cardiorespiratory responses of summer flounder Paralichthys dentatus to hypoxia at two temperatures. J Fish Biol 81(3):1043–1058. doi:10.1111/j.1095-8649.2012.03380.x

    Article  CAS  PubMed  Google Scholar 

  • Castro-Santos T, Haro A (2005) Biomechanics and fisheries conservation. Fish Physiol 23:469–523. doi:10.1016/S1546-5098(05)23012-1

    Article  Google Scholar 

  • Dorcas ME, Hopkins WA, Roe JH (2004) Effects of body mass and temperature on standard metabolic rate in the eastern diamondback rattlesnake (Crotalus adamanteus). J Inf 1:145–151. doi:10.1643/CP-03-074R1

    Google Scholar 

  • Dupont-Prinet A, Chatain B, Grima L, Vandeputte M, Claireaux G, McKenzie D (2010) Physiological mechanisms underlying a trade-off between growth rate and tolerance of feed deprivation in the European sea bass (Dicentrarchus labrax). J Exp Biol 213(7):1143–1152. doi:10.1242/jeb.037812

    Article  CAS  PubMed  Google Scholar 

  • Dupont-Prinet A, Vagner M, Chabot D, Audet C, MacLatchey D (2013) Impact of hypoxia on the metabolism of Greenland halibut (Reinhardtius hippoglossoides). Can J Fish Aquat Sci 70(3):461–469. doi:10.1139/cjfas-2012-0327

    Article  CAS  Google Scholar 

  • Essington TE, Kitchell JF, Walters CJ (2001) The von Bertalanffy growth function, bioenergetics, and the consumption rates of fish. Can J Fish Aquat Sci 58(11):2129–2138. doi:10.1139/f01-151

    Article  Google Scholar 

  • Farrell A, Hinch S, Cooke S, Patterson D, Crossin G, Lapointe M, Mathes M (2008) Pacific salmon in hot water: applying aerobic scope models and biotelemetry to predict the success of spawning migrations. Physiol Biochem Zool 81(6):697–709. doi:10.1086/592057

    Article  CAS  PubMed  Google Scholar 

  • Frederich M, Pörtner HO (2000) Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am J Physiol Regul Integr Comp Physiol 279(5):R1531–R1538

    CAS  PubMed  Google Scholar 

  • Frisk M, Skov PV, Steffensen JF (2012) Thermal optimum for pikeperch (Sander lucioperca) and the use of ventilation frequency as a predictor of metabolic rate. Aquaculture 324:151–157. doi:10.1016/j.aquaculture.2011.10.024

    Article  Google Scholar 

  • Fry F (1971) The effect of environmental factors on the physiology of fish. Fish Physiol 6:1–98. doi:10.1016/S1546-5098(08)60146-6

    Article  CAS  Google Scholar 

  • Fu SJ, Xie XJ, Cao ZD (2005a) Effect of feeding level and feeding frequency on specific dynamic action in Silurus meridionalis. J Fish Biol 67(1):171–181. doi:10.1111/j.0022-1112.2005.00722.x

    Article  Google Scholar 

  • Fu SJ, Xie XJ, Cao ZD (2005b) Effect of meal size on postprandial metabolic response in southern catfish (Silurus meridionalis). Comp Biochem Physiol A Mol Integr Physiol 140(4):445–451. doi:10.1016/j.cbpb.2005.02.008

    Article  CAS  PubMed  Google Scholar 

  • Gnaiger E (1983) Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. In: Gnaiger E, Forstner H (eds) Polarographic oxygen sensors. Springer, Berlin, pp 337–345. doi:10.1007/978-3-642-81863-9_30

  • Guinea J, Fernandez F (1997) Effect of feeding frequency, feeding level and temperature on energy metabolism in Sparus aurata. Aquaculture 148(2–3):125–142. doi:10.1016/S0044-8486(96)01424-X

    Article  Google Scholar 

  • Hansson S, Rudstam LG, Kitchell JF, Peppard P, Hildén M, Johnson B (1996) Predation rates by North Sea cod (Gadus morhua)—predictions from models on gastric evacuation and bioenergetics. ICES J Mar Sci 53(1):107–114. doi:10.1006/jmsc.1996.0010

    Article  Google Scholar 

  • Harlow HJ, Hillman SS, Hoffman M (1976) The effect of temperature on digestive efficiency in the herbivorous lizard, Dipsosaurus dorsalis. J Comp Physiol B Biochem Syst Environ Physiol 111(1):1–6. doi:10.1007/BF00691105

    Article  Google Scholar 

  • Hokanson KE, Kleiner CF, Thorslund TW (1977) Effects of constant temperatures and diel temperature fluctuations on specific growth and mortality rates and yield of juvenile rainbow trout, Salmo gairdneri. J Fish Board Can 34(5):639–648. doi:10.1139/f77-100

    Article  Google Scholar 

  • Jobling M (1985) Growth. In: Wootton RJ, Tytler P, Calow P (eds) Fish energetics: new perspectives. Croom Helm, London, pp 213–230

    Chapter  Google Scholar 

  • Jobling M (1994) Fish bioenergetics. Chapman & Hall, London

    Google Scholar 

  • Jobling M, Davies PS (1980) Effects of feeding on metabolic-rate, and the specific dynamic action in plaice, Pleuronectes-Platessa L. J Fish Biol 16(6):629–638. doi:10.1111/j.1095-8649.1980.tb03742.x

    Article  Google Scholar 

  • Jordan AD, Steffensen JF (2007) Effects of ration size and hypoxia on specific dynamic action in the cod. Physiol Biochem Zool 80(2):178–185. doi:10.1086/510565

    Article  PubMed  Google Scholar 

  • Kalarani V, Davies RW (1994) The bioenergetic costs of specific dynamic action and ammonia excretion in a freshwater predatory leech Nephelopsis obscura. Comp Biochem Physiol Part A Physiol 108(4):523–531. doi:10.1016/0300-9629(94)90336-0

    Article  CAS  Google Scholar 

  • Koenker R (2005) Quantile regression, vol 38. Cambridge university press, Cambridge

    Book  Google Scholar 

  • Koenker R (2011) Additive models for quantile regression: model selection and confidence bandaids. Braz J Probab Stat 25(3):239–262. doi:10.1214/10-BJPS131

    Article  Google Scholar 

  • Kofuji PYM, Akimoto A, Hosokawa H, Masumoto T (2005) Seasonal changes in proteolytic enzymes of yellowtail Seriola quinqueradiata (Temminck & Schlegel; Carangidae) fed extruded diets containing different protein and energy levels. Aquac Res 36(7):696–703. doi:10.1111/j.1365-2109.2005.01276.x

    Article  CAS  Google Scholar 

  • Lannig G, Bock C, Sartoris FJ, Pörtner HO (2004) Oxygen limitation of thermal tolerance in cod, Gadus morhua L., studied by magnetic resonance imaging and on-line venous oxygen monitoring. Am J Physiol Regul Integr Comp Physiol 287(4):R902–R910

    Article  CAS  PubMed  Google Scholar 

  • Luo Y, Xie X (2008) Effects of temperature on the specific dynamic action of the southern catfish, Silurus meridionalis. Comp Biochem Physiol A Mol Integr Physiol 149(2):150–156. doi:10.1016/j.cbpa.2007.11.003

    Article  PubMed  Google Scholar 

  • McCue MD (2006) Specific dynamic action: a century of investigation. Comp Biochem Physiol A Mol Integr Physiol 144(4):381–394. doi:10.1016/j.cbpa.2006.03.011

    Article  CAS  PubMed  Google Scholar 

  • McKenzie DJ, Estivales G, Svendsen JC, Steffensen JF, Agnèse J-F (2013) Local adaptation to altitude underlies divergent thermal physiology in tropical killifishes of the genus Aphyosemion. PLoS One 8(1):e54345. doi:10.1371/journal.pone.0054345

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Neuheimer A, Thresher R, Lyle J, Semmens J (2011) Tolerance limit for fish growth exceeded by warming waters. Nat Clim Chang 1(2):110–113. doi:10.1038/nclimate1084

    Article  Google Scholar 

  • Olsen R, Ringø E (1998) The influence of temperature on the apparent nutrient and fatty acid digestibility of Arctic charr, Salvelinus alpinus L. Aquac Res 29(10):695–701. doi:10.1046/j.1365-2109.1998.29100695.x

    Article  Google Scholar 

  • Pace SA (2013) Feeding frequency and water temperature impact apparent digestibility coefficients of sablefish (Anoplopoma fimbria). Dissertation, University of British Columbia

  • Pannevis MC, Houlihan DF (1992) The energetic cost of protein synthesis in isolated hepatocytes of rainbow trout (Oncorhynchus mykiss). J Comp Physiol B 162(5):393–400

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Casanova JC, Lall SP, Gamperl AK (2010) Effects of dietary protein and lipid level, and water temperature, on the post-feeding oxygen consumption of Atlantic cod and haddock. Aquac Res 41(2):198–209. doi:10.1111/j.1365-2109.2009.02318.x

    Article  Google Scholar 

  • Pérez-Rodríguez A, Saborido-Rey F (2012) Food consumption of Flemish Cap cod Gadus morhua and redfish Sebastes sp. using generic bioenergetic models. Northwest Atlantic Fisheries Organization (NAFO) Document 12/68, Serial No. N 6136

  • Pirozzi I, Booth MA (2009) The effect of temperature and body weight on the routine metabolic rate and postprandial metabolic response in mulloway, Argyrosomus japonicus. Comp Biochem Physiol Part A Mol Integr Physiol 154(1):110–118. doi:10.1016/j.cbpa.2009.05.010

    Article  Google Scholar 

  • Pörtner HO (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88(4):137–146. doi:10.1007/s001140100216

    Article  PubMed  Google Scholar 

  • Pörtner HO (2002) Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comp Biochem Physiol A Mol Integr Physiol 132(4):739–761. doi:10.1016/S1095-6433(02)00045-4

    Article  PubMed  Google Scholar 

  • Pörtner HO (2010) Oxygen-and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol 213(6):881–893. doi:10.1242/jeb.037523

    Article  PubMed  Google Scholar 

  • Pörtner HO, Farrell AP (2008) Physiology and Climate Change. Science 322(5902):690–692. doi:10.1126/science.1163156

    Article  PubMed  Google Scholar 

  • Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315(5808):95–97. doi:10.1126/science.1135471

    Article  PubMed  Google Scholar 

  • Satoh K, Kimoto K, Hitaka E (2004) Effect of water temperature on the protein digestibility of extruded pellet, single moist pellet and Oregon moist pellet in one-year-old yellowtail. Nippon Suisan Gakk 70(5):758–763. doi:10.2331/suisan.70.758

    Article  Google Scholar 

  • Saunders RL (1963) Respiration of the Atlantic cod. J Fish Res Board Can 20(2):373–386. doi:10.1139/f63-031

    Article  Google Scholar 

  • Schurmann H, Steffensen JF (1997) Effects of temperature, hypoxia and activity on the metabolism of juvenile Atlantic cod. J Fish Biol 50(6):1166–1180. doi:10.1111/j.1095-8649.1997.tb01645.x

  • Secor SM (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B Biochem Syst Environ Physiol 179(1):1–56. doi:10.1007/s00360-008-0283-7

    Article  Google Scholar 

  • Secor SM, Boehm M (2006) Specific dynamic action of ambystomatid salamanders and the effects of meal size, meal type, and body temperature. Physiol Biochem Zool 79(4):720–735. doi:10.1086/505511

    Article  PubMed  Google Scholar 

  • Shi-Jian F, Xiao-Jun X, Zhen-Dong C (2005) Effect of dietary composition on specific dynamic action in southern catfish Silurus meridionalis Chen. Aquac Res 36(14):1384–1390. doi:10.1111/j.1365-2109.2005.01356.x

    Article  Google Scholar 

  • Singh-Renton S, Bromley P (1996) Effects of temperature, prey type and prey size on gastric evacuation in small cod and whiting. J Fish Biol 49(4):702–713. doi:10.1111/j.1095-8649.1996.tb00066.x

    Article  Google Scholar 

  • Smit H (1967) Influence of temperature on the rate of gastric juice secretion in the brown bullhead, Ictalurus nebolosus. Comp Biochem Physiol 21(1):125–132

    Article  Google Scholar 

  • Soofiani NM, Hawkins AD (1982) Energetic costs at different levels of feeding in juvenile cod, Gadus-morhua L. J Fish Biol 21(5):577–592. doi:10.1111/j.1095-8649.1982.tb02861.x

    Article  Google Scholar 

  • Steffensen JF (1989) Some errors in respirometry of aquatic breathers—how to avoid and correct for them. Fish Physiol Biochem 6(1t):49–59. doi:10.1007/BF02995809

    Article  CAS  PubMed  Google Scholar 

  • Steffensen JF, Schurmann H, Bushnell PG (1994) Oxygen-consumption in 4 species of teleosts from Greenland—no evidence of metabolic cold adaptation. Polar Biol 14(1):49–54. doi:10.1007/BF00240272

    Article  Google Scholar 

  • Svendsen JC, Steffensen JF, Aarestrup K, Frisk M, Etzerodt A, Jyde M (2012) Excess posthypoxic oxygen consumption in rainbow trout (Oncorhynchus mykiss): recovery in normoxia and hypoxia. Can J Zool 90(1):1–11. doi:10.1139/z11-095

    Article  CAS  Google Scholar 

  • Svendsen JC, Banet AI, Christensen RH, Steffensen JF, Aarestrup K (2013) Effects of intraspecific variation in reproductive traits, pectoral fin use and burst swimming on metabolic rates and swimming performance in the Trinidadian guppy (Poecilia reticulata Peters). J Exp Biol 216:3564–3574. doi:10.1242/jeb.083089

    Article  PubMed  Google Scholar 

  • Team RDC (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Tirsgaard B, Behrens JW, Steffensen JF (2014) The effect of temperature and body size on metabolic scope of activity in juvenile Atlantic cod. Comp Biochem Physiol Part A Mol Integr Physiol, Gadus morhua L. doi:10.1016/j.cbpa.2014.09.033

    Google Scholar 

  • Tyler A (1970) Rates of gastric emptying in young cod. J Fish Board Can 27(7):1177–1189. doi:10.1139/f70-140

    Article  Google Scholar 

  • Vanella FA, Boy CC, Lattuca ME, Calvo J (2010) Temperature influence on post-prandial metabolic rate of sub-Antarctic teleost fish. Comp Biochem Physiol A Mol Integr Physiol 156(2):247–254. doi:10.1016/j.cbpa.2010.02.006

    Article  PubMed  Google Scholar 

  • Von Herbing IH, White L (2002) The effects of body mass and feeding on metabolic rate in small juvenile Atlantic cod. J Fish Biol 61(4):945–958. doi:10.1111/j.1095-8649.2002.tb01854.x

    Article  Google Scholar 

  • Wang T, Zaar M, Arvedsen S, Vedel-Smith C, Overgaard J (2002) Effects of temperature on the metabolic response to feeding in Python molurus. Comp Biochem Physiol A Mol Integr Physiol 133(3):519–527. doi:10.1016/S1095-6433(02)00250-7

    Article  PubMed  Google Scholar 

  • Ware D (1982) Power and evolutionary fitness of teleosts. Can J Fish Aquat Sci 39(1):3–13. doi:10.1139/f82-002

    Article  Google Scholar 

  • Windell JT, Foltz JW, Sarokon JA (1978) Effect of fish size, temperature, and amount fed on nutrient digestibility of a pelleted diet by rainbow trout, Salmo gairdneri. Trans Am Fish Soc 107(4):613–616. doi:10.1577/1548-8659(1978)107<613:EOFSTA>2.0.CO;2

    Article  CAS  Google Scholar 

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Acknowledgments

This study was part of the project SUNFISH (sustainable fisheries, climate change and the North Sea ecosystem), and financially supported by the Danish Council for Strategic Research [Grant Number 09-063096] and Department of Biology, University of Copenhagen [Grant Number 102-0218/11-5550]. Jon Christian Svendsen was supported by the Foundation for Science and Technology (FCT) in Portugal (Grant Number SFRH/BPD/89473/2012). We thank an anonymous reviewer for helpful and constructive comments on an earlier version of the manuscript.

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Tirsgaard, B., Svendsen, J.C. & Steffensen, J.F. Effects of temperature on specific dynamic action in Atlantic cod Gadus morhua . Fish Physiol Biochem 41, 41–50 (2015). https://doi.org/10.1007/s10695-014-0004-y

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