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Individual variation in metabolic rate, locomotion capacity and hypoxia tolerance and their relationships in juveniles of three freshwater fish species

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Abstract

Individual variations in metabolic rate, locomotion capacity and hypoxia tolerance and their relationships were investigated in three cyprinid species [crucian carp (Carassius auratus), common carp (Cyprinus carpio) and qingbo (Spinibarbus sinensis), in 60 individuals of each species]. Either the active metabolic rate (AMR) and critical swimming speed (Ucrit) (30 individuals) or critical oxygen tension (Pcrit) and loss of equilibrium (LOE) (30 individuals) were measured in each species after measuring the resting metabolic rate (RMR). Both the AMR and Ucrit were found to be significantly and positively correlated with the RMR in all three cyprinid species, indicating that high-RMR individuals have high aerobic capacity and thus good swimming performance. Pcrit was positively correlated with the RMR in all three species, whereas the LOE was highly positively correlated, weakly positively correlated and not correlated with the RMR in qingbo, common carp and crucian carp, respectively, possibly due to specialized morphological and biochemical adaptations involved in hypoxia tolerance in crucian and common carp. Crucian carp showed relatively poor swimming performance, i.e., a low Ucrit (relatively high variation), strong hypoxia tolerance, and low LOE (relatively low variation); qingbo showed relatively good swimming performance (relatively low variation) and weak hypoxia tolerance (relatively high variation); and common carp showed moderate swimming performance and relatively strong hypoxia tolerance (moderate variation). These interspecific differences may be due to the different lifestyles of these cyprinid fishes based on their associated fast–slow-flow regime and are outcomes of long-term selection.

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References

  • Auer SK, Salin K, Rudolf AM, Anderson GJ, Metcalfe NB (2015) The optimal combination of standard metabolic rate and aerobic scope for somatic growth depends on food availability. Funct Ecol 29:479–486

    Article  Google Scholar 

  • Barnes RK, King H, Carter CG (2011) Hypoxia tolerance and oxygen regulation in Atlantic salmon, Salmo salar from a Tasmanian population. Aquaculture 318:397–401

    Article  Google Scholar 

  • Bennett AF, Ruben JA (1979) Endothermy and activity in vertebrates. Science 206:649–654

    Article  CAS  PubMed  Google Scholar 

  • Biro PA, Stamps JA (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 25:653–659

  • Boldsen MM, Norin T, Malte H (2013) Temporal repeatability of metabolic rate and the effect of organmass and enzyme activity on metabolism in European eel (Anguilla anguilla). Comp Biochem Physiol A 165:22–29

    Article  CAS  Google Scholar 

  • Brett JR (1964) The respiratory metabolism and swimming performance of young sockeye salmon. J Fish Res Board Canada 21:1183–1226

    Article  Google Scholar 

  • Chabot D, Steffensen JF, Farrell AP (2016) The determination of standard metabolic rate in fishes. J Fish Biol 88:81–121

    Article  CAS  PubMed  Google Scholar 

  • Chapman LJ, Chapman CA, Nordlie FG, Rosenberger AE (2002) Physiological refugia: swamps, hypoxia tolerance and maintenance of fish diversity in the Lake Victoria region. Comp Biochem Physiol A 133:421–437

    Article  Google Scholar 

  • Chappell M, Garland TG, Saltzman W (2007) Relationships among running performance, aerobic physiology and organ mass in male Mongolian gerbils. J Exp Biol 210:4179–4197

    Article  PubMed  Google Scholar 

  • Chen BJ, Fu SJ, Cao ZD, Wang YX (2019) Effect of temperature on critical oxygen tension (Pcrit) and gill morphology in six cyprinids in the Yangtze River, China. Aquaculture 508:137–146

    Article  Google Scholar 

  • Clarke A, Fraser KPP (2004) Why does metabolism scale with temperature? Funct Ecol 18:243–251

    Article  Google Scholar 

  • Crans KD, Pranckevicius NA, Scott GR (2015) Physiological tradeoffs may underlie the evolution of hypoxia tolerance and exercise performance in sunfish (Centrarchidae). J Exp Biol 218:3264–3275

    PubMed  Google Scholar 

  • Dhillon RS, Yao L, Matey V, Chen BJ, Zhang AJ, Cao ZD, Fu SJ, Brauner CJ, Wang YXS, Richardset JG (2013) Interspecific differences in hypoxia-induced gill remodeling in carp. Physiol Biochem Zool 86:727–739

    Article  PubMed  Google Scholar 

  • Dhillon RS, Mandic M, Yao L, Cao ZD, Fu SJ, Brauner CJ, Wang YXS, Richards JG (2018) Ethanol metabolism varies with hypoxia tolerance in ten cyprinid species. J Comp Physiol B 188:283–293

    Article  CAS  PubMed  Google Scholar 

  • Fu SJ, Xie XJ, Cao ZD (2005) Effect of dietary composition on specific dynamic action in southern catfish Silurus meridionalis Chen. Aquac Res 36:1384–1390

    Article  CAS  Google Scholar 

  • Fu SJ, Cao ZD, Peng JL, Wang YX (2008) Is peak postprandial oxygen consumption positively related to growth rate and resting oxygen consumption in a sedentary catfish Silurus meridionalis? J Fish Biol 73:692–670

    Article  CAS  Google Scholar 

  • Fu SJ, Brauner CJ, Cao ZD, Richards JG, Peng JL, Dhillon R, Wang YX (2011) The effect of acclimation to hypoxia and sustained exercise on subsequent hypoxia tolerance and swimming performance in goldfish (Carassius auratus). J Exp Biol 214:2080–2088

    Article  CAS  PubMed  Google Scholar 

  • Fu SJ, Fu C, Yan GJ, Cao ZD, Zhang AJ, Pang X (2014) Interspecific variation in hypoxia tolerance, swimming performance and plasticity in cyprinids that prefer different habitats. J Exp Biol 217:590–597

    PubMed  Google Scholar 

  • Genz J, Jyde MB, Svendsen JC, Steffensen JF, Ramløv H (2013) Excess post-hypoxic oxygen consumption is independent from lactate accumulation in two cyprinid fishes. Comp Biochem Physiol A 165:54–60

    Article  CAS  Google Scholar 

  • He W, Cao ZD, Fu SJ (2015) Effect of temperature on hypoxia tolerance and its underlying biochemical mechanism in two juvenile cyprinids exhibiting distinct hypoxia sensitivities. Comp Biochem Physiol A 187:232–241

    Article  CAS  Google Scholar 

  • Jobling M (1994) Respiration and metabolism. In: Jobling M (ed) Fish bioenergetics. Chapman & Hall, London, pp 121–145

    Google Scholar 

  • Johnston IA, Bernard LM (1983) Utilization of the ethanol pathway in carp following exposure to anoxia. J Exp Biol 104:73–78

    Article  CAS  Google Scholar 

  • Killen SS, Marras S, Ryan MR, Domenici P, McKenzie DJ (2012) A relationship between metabolic rate and risk-taking behaviour is revealed during hypoxia in juvenile European sea bass. Funct Ecol 26:134–143

    Article  Google Scholar 

  • Killen SS, Glazier DS, Rezende EL, Clark TD, Atkinson D, Willener AS, Halsey L (2016) Ecological influences and morphological correlates of resting and maximal metabolic rates across teleost fish species. Am Nat 187:592–606

    Article  PubMed  Google Scholar 

  • Langerhans RB (2009) Trade-off between steady and unsteady swimming underlies predator-driven divergence in Gambusia affinis. J Evol Biol 22:1057–1075

    Article  CAS  PubMed  Google Scholar 

  • Lee CG, Farrell AP, Lotto A, MacNutt MJ, Hinch SG, Healey MC (2003) The effect of temperature on swimming performance and oxygen consumption in adult sockeye (Oncorhynchus nerka) and coho (O. Kisutch) salmon stocks. J Exp Biol 206:3239–3251

    Article  CAS  PubMed  Google Scholar 

  • Mandic M, Todgham AE, Richards JG (2009) Mechanisms and evolution of hypoxia tolerance in fish. Proc R Soc B 276:735–744

    Article  CAS  PubMed  Google Scholar 

  • Mandic M, Speers-Roesch B, Richards JG (2013) Hypoxia tolerance in sculpins is associated with high anaerobic enzyme activity in brain but not in liver or muscle. Physiol Biochem Zool 86:92–105

    Article  CAS  PubMed  Google Scholar 

  • Marras S, Claireaux G, Mckenzie DJ, Nelson JA (2010) Individual variation and repeatability in aerobic and anaerobic swimming performance of European sea bass, Dicentrarchus labrax. J Exp Biol 213:26–32

    Article  CAS  PubMed  Google Scholar 

  • Nelson J, Tang Y, Boutilier R (1996) The effects of salinity change on the exercise performance of two Atlantic cod (Gadus morhua) populations inhabiting different environments. J Exp Biol 199:1295–1309

    Article  CAS  PubMed  Google Scholar 

  • Norin T, Clark TD (2016) Measurement and relevance of maximum metabolic rate in fishes. J Fish Biol 88:122–151

    Article  CAS  PubMed  Google Scholar 

  • Norin T, Malte H (2012) Intraspecific variation in aerobic metabolic rate of fish: relations with organ size and enzyme activity in brown trout. Physiol Biochem Zool 85:645–656

    Article  PubMed  Google Scholar 

  • Pang X, Cao ZD, Fu SJ (2011) The effects of temperature on metabolic interaction between digestion and locomotion in juveniles of three cyprinid fish (Carassius auratus, Cyprinus carpio and Spinibarbus sinensis). Comp Biochem Physiol A 159:253–260

    Article  Google Scholar 

  • Pang X, Fu S, Zhang Y (2015) Individual variation in metabolism and swimming performance in juvenile black carp (Mylopharyngodon piceus) and the effects of hypoxia. Mar Freshw Behav Physiol 48:431–443

    Article  Google Scholar 

  • Pang X, Fu SJ, Zhang YG (2016) Acclimation temperature alters the relationship between growth and swimming performance among juvenile common carp (Cyprinus carpio). Comp Biochem Physiol A 199:111–119

    Article  CAS  Google Scholar 

  • Pang X, Shao F, Ding SH, Fu SJ, Zhang YG (2020) Interspecific differences and ecological correlations of energy metabolism traits in freshwater fishes. Funct Ecol 34:616–630

    Article  Google Scholar 

  • Reidy SP, Nelson JA, Tang Y, Kerr SR (1995) Post-exercise metabolic rate in Atlantic cod and its dependence upon the method of exhaustion. J Fish Biol 47:377–386

    Article  Google Scholar 

  • Reidy SP, Kerr SR, Nelson JA (2000) Aerobic and anaerobic swimming performance of individual Atlantic cod. J Exp Biol 203:347–357

    Article  CAS  PubMed  Google Scholar 

  • Rezende EL (2013) Evolution: better oxygen delivery. Science 340:1293–1294

    Article  PubMed  Google Scholar 

  • Richards JG (2011) Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia. J Exp Biol 214:191–199

    Article  PubMed  Google Scholar 

  • Rogers NJ, Urbina MA, Reardon EE, Mckenzie DJ, Wilson RW (2016) A new analysis of hypoxia tolerance in fishes using a database of critical oxygen level (Pcrit). Conserv Physiol 4:cow012

    Article  PubMed  PubMed Central  Google Scholar 

  • Schurmann H, Steffensen JF (1997) Effects of temperature, hypoxia and activity on the metabolism of juvenile Atlantic cod. J Fish Biol 50:1166–1180

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Svendsen JC, Tudorache C, Jordan AD, Steffensen JF, Aarestrup K, Domenici P (2010) Partition of aerobic and anaerobic swimming costs related to gait transitions in a labriform swimmer. J Exp Biol 213:2177–2183

    Article  PubMed  Google Scholar 

  • Svendsen JC, Tirsgaard B, Cordero G, Steffensen JF (2015) Intraspecific variation in aerobic and anaerobic locomotion: gilthead sea bream (Sparus aurata) and Trinidadian guppy (Poecilia reticulata) do not exhibit a trade-off between maximum sustained swimming speed and minimum cost of transport. Front Physiol 6:43

    Article  PubMed  PubMed Central  Google Scholar 

  • Ultsch GR, Boschung H, Ross MJ (1978) Metabolism, critical oxygen tension, and habitat selection in darters (Etheostoma). Ecology 59:99–107

    Article  Google Scholar 

  • Wood CM (2018) The fallacy of the Pcrit—are there more useful alternatives? J Exp Biol 221:jeb163717

    Article  PubMed  Google Scholar 

  • Yan GJ, He XK, Cao ZD, Fu SJ (2013) An interspecific comparison between morphology and swimming performance in cyprinids. J Evol Biol 26:1802–1815

    Article  PubMed  Google Scholar 

  • Yeager DP, Ultsch GR (1989) Physiological regulation and conformation: a basic program for the determination of critical points. Physiol Zool 62:888–907

  • Zhang W, Cao ZD, Peng JL, Chen BJ, Fu SJ (2010) The effects of dissolved oxygen level on the metabolic interaction between digestion and locomotion in juvenile southern catfish (Silurus meridionalis Chen). Comp Biochem Physiol A 157:212–219

    Article  Google Scholar 

Download references

Acknowledgements

This study was funded by the National Natural Science Foundation of China (31702020) and the Natural Science Foundation of Chongqing (cstc2020jcyj-msxmX0479; cstc2018jcyjAX0150).

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Correspondence to Shi-Jian Fu.

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Communicated by B. Pelster.

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Pang, X., Pu, DY., Xia, DY. et al. Individual variation in metabolic rate, locomotion capacity and hypoxia tolerance and their relationships in juveniles of three freshwater fish species. J Comp Physiol B 191, 755–764 (2021). https://doi.org/10.1007/s00360-021-01382-w

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