Abstract
In order to evaluate the effects of acute temperature exposure on the swimming performance of rainbow trout (Oncorhynchus mykiss), the critical swimming speed (Ucrit) and oxygen consumption rates (MO2) were determined at different temperatures (13.2, 18.4, and 22.5 °C). The Ucrit and MO2 of different body mass (109.44, 175.74, and 249.42 g) fish were also obtained at 13.4 °C. The Ucrit first increased as the temperature increased from 13.2 to 15.2 °C, which was calculated to be the optimal temperature for the Ucrit, and then decreased with increasing temperature. The optimal swimming speed (Uopt) showed a similar trend to the Ucrit. At a given swimming speed, the MO2 and cost of transport (COT) were significantly higher at 22.5 than at 13.2 °C, suggesting the energy utilization efficiency decreased with increasing temperature. The absolute values of Ucrit and Uopt increased as the body mass increased from 109.44 to 249.42 g, whereas the relative values decreased. Although not statistically significant, the maximum metabolic rate (MMR) tended to increase with temperature but decrease with body mass. Results can be of value in understanding the behavioral and physiological response of rainbow trout to acute temperature change.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article.
References
Altimiras J, Axelsson M, Claireaux G, Lefrancois C, Mercier C, Farrell AP (2002) Cardiorespiratory status of triploid brown trout during swimming at two acclimation temperatures. J Fish Biol 60:102–116
Beamish FWH (1978) Swimming capacity. In: Hoar WS, Randall DJ (eds) Fish physiology VII locomotion. Academic Press, New York, pp 101–187
Bellehumeur K, Lapointe D, Cooke SJ, Moon TW (2016) Exposure to sublethal levels of PCB-126 impacts fuel metabolism and swimming performance in rainbow trout. Comp Biochem Physiol B 199:97–104. https://doi.org/10.1016/j.cbpb.2016.01.005
Blair SD, Glover CN (2019) Acute exposure of larval rainbow trout (Oncorhynchus mykiss) to elevated temperature limits hsp70b expression and influences future thermotolerance. Hydrobiologia 836:155–167. https://doi.org/10.1007/s10750-019-3948-1
Brett JR (1964) The respiratory metabolism and swimming performance of young sockeye salmon. J Fish Res Board Can 21:1183–1226
Brett JR (1971) Energetic responses of salmon to temperature a study of some thermal relation in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerkd). Am Zool 11:99–113
Brett JR, Glass N (1973) Metabolic rates and critical swimming speeds of sockeye salmon (Oncorhynchus nerka) in relation to size and temperature. J Fish Res Board Can 30:379–387. https://doi.org/10.1139/f73-068
Brijs J, Gräns A, Hjelmstedt P, Sandblom E, Van Nuland N, Berg C, Axelsson M (2018) In vivo aerobic metabolism of the rainbow trout gut and the effects of an acute temperature increase and stress event. J Exp Biol 221:jeb180703. https://doi.org/10.1242/jeb.180703
Cai L, Taupier R, Johnson D, Tu Z, Liu G, Huang Y (2013) Swimming capability and swimming behavior of juvenile Acipenser schrenckii. J Exp Zool A 319:149–155. https://doi.org/10.1002/jez.1780
Christensen EAF, Illing B, Iversen NS, Johansen JL, Domenici P, Steffensen JF (2018) Effects of salinity on swimming performance and oxygen consumption rate of shiner perch Cymatogaster aggregata. J Exp Mar Biol Ecol 504:32–37. https://doi.org/10.1016/j.jembe.2018.04.002
Claireaux G, Couturier C, Groison AL (2006) Effect of temperature on maximum swimming speed and cost of transport in juvenile European sea bass (Dicentrarchus labrax). J Exp Biol 209:3420–3428. https://doi.org/10.1242/jeb.02346
Coughlin DJ, Wilson LT, Kwon ES, Travitz LS (2020) Thermal acclimation of rainbow trout myotomal muscle, can trout acclimate to a warming environment? Comp Biochem Physiol A 245:110702. https://doi.org/10.1016/j.cbpa.2020.110702
Dickson KA, Donley JM, Sepulveda C, Bhoopat L (2002) Effects of temperature on sustained swimming performance and swimming kinematics of the chub mackerel Scomber japonicus. J Exp Biol 205:969–980
Farrell AP, Johansen JA, Suarez RK (1991) Effects of exercise-training on cardiac performance and muscle enzymes in rainbow trout, Oncorhynchus mykiss. Fish Physiol Biochem 9:303–312. https://doi.org/10.1007/BF02265151
Farrell AP, Gamperl AK, Hicks JMT, Shiels HA, Jain KE, Sciences B (1996) Maximum cardiac performance of rainbow trout (Oncorhynchus mykiss) at temperatures approaching their upper lethal limit. J Exp Biol 199:663–672
Fry FEJ, Hart JS (1948) The relation of temperature to oxygen consumption in the goldfish. Biol Bull 94:66–77
Fuiman LA, Batty RS (1997) What a drag it is getting cold: partitioning the physical and physiological effects of temperature on fish swimming. J Exp Biol 200:1745–1755
Glova GJ, McInerney JE (1977) Critical swimming speeds of coho salmon (Oncorhynchus keta) fry to smolt stages in relation to salinity and temperature. J Fish Res Board Can 34:151–154
Goulding AT, Shelley LK, Ross PS, Kennedy CJ (2013) Reduction in swimming performance in juvenile rainbow trout (Oncorhynchus mykiss) following sublethal exposure to pyrethroid insecticides. Comp Biochem Physiol C 157:280–286. https://doi.org/10.1016/j.cbpc.2013.01.001
Guan L, Snelgrove PVR, Gamperl AK (2008) Ontogenetic changes in the critical swimming speed of Gadus morhua (Atlantic cod) and Myoxocephalus scorpius (shorthorn sculpin) larvae and the role of temperature. J Exp Mar Biol Ecol 360:31–38. https://doi.org/10.1016/j.jembe.2008.03.006
Hammer C (1995) Fatigue and exercise tests with fish. Comp Biochem Physiol A 112:1–20. https://doi.org/10.1016/0300-9629(95)00060-K
He X, Lu S, Liao M, Zhu X, Zhang M, Li S, You X (2013a) Effects of age and size on critical swimming speed of juvenile Chinese sturgeon Acipenser sinensis at seasonal temperatures. J Fish Biol 82:1047–1056. https://doi.org/10.1111/j.1095-8649.2012.12015.x
He W, Xia W, Cao ZD, Fu SJ (2013b) The effect of prolonged exercise training on swimming performance and the underlying biochemical mechanisms in juvenile common carp (Cyprinus carpio). Comp Biochem Physiol A 166:308–315. https://doi.org/10.1016/j.cbpa.2013.07.003
Huang J, Li Y, Liu Z, Kang Y, Wang J (2018) Transcriptomic responses to heat stress in rainbow trout Oncorhynchus mykiss head kidney. Fish Shellfish Immunol 82:32–40. https://doi.org/10.1016/j.fsi.2018.08.002
Hunt von Herbing I (2002) Effects of temperature on larval fish swimming performance: the importance of physics to physiology. J Fish Biol 61:865–876. https://doi.org/10.1006/jfbi.2002.2118
Jain KE, Hamilton JC, Farrell AP (1997) Use of a ramp velocity test to measure critical swimming speed in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A 117:441–444. https://doi.org/10.1016/S0300-9629(96)00234-4
Jia Y, Cavileer TD, Nagler JJ (2016) Acute hyperthermic responses of heat shock protein and estrogen receptor mRNAs in rainbow trout hepatocytes. Comp Biochem Physiol A 201:156–161. https://doi.org/10.1016/j.cbpa.2016.04.023
Joaquim N, Wagner GN, Gamperl AK (2004) Cardiac function and critical swimming speed of the winter flounder (Pleuronectes americanus) at two temperatures. Comp Biochem Physiol A 138:277–285. https://doi.org/10.1016/j.cbpb.2004.03.016
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. https://doi.org/10.1242/jeb.00547
Li XM, Cao ZD, Peng JL, Fu SJ (2010) The effect of exercise training on the metabolic interaction between digestion and locomotion in juvenile darkbarbel catfish (Peltebagrus vachelli). Comp Biochem Physiol A 156:67–73. https://doi.org/10.1016/j.cbpa.2009.12.022
MacNutt M, Hinch S, Farrell A, Topp S (2004) The effect of temperature and acclimation period on repeat swimming performance in cutthroat trout. J Fish Biol 65:342–353. https://doi.org/10.1111/j.1095-8649.2004.00453.x
Mcdonnell LH, Chapman LJ (2016) Effects of thermal increase on aerobic capacity and swim performance in a tropical inland fish. Comp Biochem Physiol A 199:62–70. https://doi.org/10.1016/j.cbpa.2016.05.018
Myrick CA, Cech JJ (2000) Temperature influences on California rainbow trout physiological performance. Fish Physiol Biochem 22:245–254. https://doi.org/10.1023/A:1007805322097
Nelson JA (2016) Oxygen consumption rate v rate of energy utilization of fishes: a comparison and brief history of the two measurements. J Fish Biol 88:10–25. https://doi.org/10.1111/jfb.12824
Nilsson GE, Crawley N, Lunde IG, Munday PL (2009) Elevated temperature reduces the respiratory scope of coral reef fishes. Glob Chang Biol 15:1405–1412. https://doi.org/10.1111/j.1365-2486.2008.01767.x
Norin T, Malte H, Clark TD (2014) Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures. J Exp Biol 217:244–251. https://doi.org/10.1242/jeb.089755
Oldham T, Nowak B, Hvas M, Oppedal F (2019) Metabolic and functional impacts of hypoxia vary with size in Atlantic salmon. Comp Biochem Physiol A 231:30–38. https://doi.org/10.1016/j.cbpa.2019.01.012
Palstra AP, Planas JV (2011) Fish under exercise. Fish Physiol Biochem 37:259–272. https://doi.org/10.1007/s10695-011-9505-0
Palstra AP, Mes D, Kusters K, Roques JAC, Flik G, Kloet K, Blonk RJW (2015) Forced sustained swimming exercise at optimal speed enhances growth of juvenile yellowtail kingfish (Seriola lalandi). Front Physiol 5:1–11. https://doi.org/10.3389/fphys.2014.00506
Pang X, Yuan XZ, Cao ZD, Fu SJ (2013) The effects of temperature and exercise training on swimming performance in juvenile qingbo (Spinibarbus sinensis). J Comp Physiol B 183:99–108. https://doi.org/10.1007/s00360-012-0690-7
Plaut I (2001) Critical swimming speed: its ecological relevance. Comp Biochem Physiol A 131:41–50. https://doi.org/10.1016/S1095-6433(01)00462-7
Pörtner HO (2001) Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146
Randall D, Brauner C (1991) Effects of environmental factors on exercise in fish. J Exp Biol 160:113–126
Reidy SP, Kerr SR, Nelson JA (2000) Aerobic and anaerobic swimming performance of individual Atlantic cod. J Exp Biol 203:347–357
Roche DG, Binning SA, Bosiger Y, Johansen JL, Rummer JL (2013) Finding the best estimates of metabolic rates in a coral reef fish. J Exp Biol 216:2103–2110. https://doi.org/10.1242/jeb.082925
Rome LC, Funke RP, Alexander RM (1990) The influence of temperature on muscle velocity and sustained performance in swimming carp. J Exp Biol 154:163–178
Rosengren M, Thörnqvist PO, Johnsson JI, Sandblom E, Winberg S, Sundell K (2017) High risk no gain-metabolic performance of hatchery reared Atlantic salmon smolts, effects of nest emergence time, hypoxia avoidance behaviour and size. Physiol Behav 175:104–112. https://doi.org/10.1016/j.physbeh.2017.03.028
Sandblom E, Gräns A, Axelsson M, Seth H (2014) Temperature acclimation rate of aerobic scope and feeding metabolism in fishes: implications in a thermally extreme future. Proc R Soc B Biol Sci 281(1794):20141490. https://doi.org/10.1098/rspb.2014.1490
Skov PV, Larsen BK, Frisk M, Jokumsen A (2011) Effects of rearing density and water current on the respiratory physiology and haematology in rainbow trout, Oncorhynchus mykiss at high temperature. Aquaculture 319:446–452. https://doi.org/10.1016/j.aquaculture.2011.07.008
Tirsgaard B, Behrens JW, Steffensen JF (2015) The effect of temperature and body size on metabolic scope of activity in juvenile Atlantic cod Gadus morhua L. Comp Biochem Physiol A 179:89–94. https://doi.org/10.1016/j.cbpa.2014.09.033
Verhille CE, English KK, Cocherell DE, Farrell AP, Fangue NA (2016) High thermal tolerance of a rainbow trout population near its southern range limit suggests local thermal adjustment. Conserv Physiol 4:cow057. https://doi.org/10.1093/conphys/cow057
Wang ZM, Yang YH (2002) Cold water fish culture in China. In: Petr T, Swar DB (eds) Cold water fisheries in the trans-himalayan countries. FAO Fisheries Technical Paper No. 431, Rome, pp 97–106
Webb PW (1984) Body form, locomotion and foraging in aquatic vertebrates. Am Zool 24:107–120
Webb PW, Kostecki PT, Don Stevens E (1984) The effect of size and swimming speed on locomotor kinematics of rainbow trout. J Exp Biol 109:77–95
Yan GJ, He XK, Cao ZD, Fu SJ (2012) The trade-off between steady and unsteady swimming performance in six cyprinids at two temperatures. J Therm Biol 37(6):424–431. https://doi.org/10.1016/j.jtherbio.2012.04.006
Yu XM, Chen L, Cui WD, Xing BB, Zhuang X, Zhang GS (2018) Effects of acute temperature and salinity changes, body length and starvation on the critical swimming speed of juvenile tiger puffer, Takifugu rubripes. Fish Physiol Biochem 44:311–318
Acknowledgments
The authors would like to thank the anonymous reviewers for their helpful comments.
Authors’ contributions (all authors should be included)
X.M.Y. conceived and designed the experiments. L.M.Y. and H.Q.L. carried out the experiments. L.C. and M.L.W. analyzed the data and created the tables and figures. L.M.Y. and X.M.Y. wrote the article.
Code availability
Not applicable.
Funding
This work was supported by funds from Support High-Level Talent Innovation and Entrepreneurship Project of Dalian (2016RQ067), Educational Department of Liaoning Province (DL201703), and Key Laboratory of Mariculture & Stock Enhancement in North China’s Sea, Ministry of Agriculture and Rural Affairs, Dalian Ocean University, P. R. China (2018KF20).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no conflict of interest.
Ethical approval
All animal procedures used complied with the Guidelines for the Care and Use of Laboratory Animals in China and were approved by the Ethics Committee of Dalian Ocean University.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Yin, L., Chen, L., Wang, M. et al. An acute increase in water temperature can decrease the swimming performance and energy utilization efficiency in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 47, 109–120 (2021). https://doi.org/10.1007/s10695-020-00897-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-020-00897-3