Fish Physiology and Biochemistry

, Volume 43, Issue 5, pp 1279–1287 | Cite as

Effects of temperature and fatigue on the metabolism and swimming capacity of juvenile Chinese sturgeon (Acipenser sinensis)

  • Xi Yuan
  • Yi-hong Zhou
  • Ying-ping Huang
  • Wen-tao Guo
  • David Johnson
  • Qing Jiang
  • Jin-jie Jing
  • Zhi-ying Tu
Article
  • 263 Downloads

Abstract

Chinese sturgeon (Acipenser sinensis) is a critically endangered species. A flume-type respirometer, with video, was used to conduct two consecutive stepped velocity tests at 10, 15, 20, and 25 °C. Extent of recovery was measured after the 60-min recovery period between trials, and the recovery ratio for critical swimming speed (U crit) averaged 91.88% across temperatures. Temperature (T) effects were determined by comparing U crit, oxygen consumption rate (MO 2), and tail beat frequency (TBF) for each temperature. Results from the two trials were compared to determine the effect of exercise. The U crit occurring at 15 °C in both trials was significantly higher than that at 10 and 25 °C (p < 0.05). The U crit was plotted as a function of T and curve-fitting allowed calculation of the optimal swimming temperature 3.28 BL/s at 15.96 °C (trial 1) and 2.98 BL/s at 15.85 °C (trial 2). In trial 1, MO 2 increased rapidly with U, but then declined sharply as swimming speed approached U crit. In trial 2, MO 2 increased more slowly, but continuously, to U crit. TBF was directly proportional to U and the slope (dTBF/dU) for trial 2 was significantly lower than that for trial 1. The inverse slope (tail beats per body length, TB/BL) is a measure of swimming efficiency and the significant difference in slopes implies that the exercise training provided by trial 1 led to a significant increase in swimming efficiency in trial 2.

Keywords

Chinese sturgeon Temperature Swimming performance Oxygen consumption 

Notes

Acknowledgements

We are grateful to Prof. Liu Jing-xia for grammar revision, and the two anonymous reviewers provided constructive comments. This research has been supported by the National Major Science and Technology Program for Water Pollution Control and Management (Grant number 2012ZX07104-003-04), Hubei Province Innovation Group Project (Grant number 2015CFA021), National Nature Science Foundation of China (Grant numbers 51309140, 51679126, 51609155), and Hubei Key Laboratory of Three Gorges Project for Conservation of Fishes (Grant number 0704102).

References

  1. Alexander RM (1989) Optimization and gaits in the locomotion of vertebrates. Physiol Rev 69(4):1199–1227Google Scholar
  2. Bagatto B, Pelster B, Burggren WW (2001) Growth and metabolism of larval zebrafish: effects of swim training. J Exp Biol 204(24):4335–4343PubMedGoogle Scholar
  3. Brett JR (1964) The respiratory metabolism and swimming performance of young Sockeye Salmon. J Fish Res Board Can 21(5):1183–1226Google Scholar
  4. Cai L, Chen L, David J, Liu GY, Prashant M, Fang M (2014) Integrating water flow, locomotor performance and respiration of Chinese sturgeon during multiple fatigue-recovery cycles. PLoS One 9(4):e94345. doi: 10.1371/journal.pone.0094345 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cano JM and Nicieza AG (2006) Temperature, metabolic rate, and constraints on locomotor performance in ectotherm vertebrates. Funct Ecol 20(3):464–470. doi: 10.1111/j.1365-2435.2006.01129.x
  6. Cech JJ, Mitchell SJ, Wragg TE (1984) Comparative growth of juvenile white sturgeon and striped bass: effects of temperature and hypoxia. Estuar Coasts 7(1):12–18. doi: 10.2307/1351952 CrossRefGoogle Scholar
  7. Chen YB, Wu BF (2011) Impact analysis of the Three-Gorges Project on the spawning of Chinese sturgeon Acipenser sinensis. J Appl Ichthyol 27(2):383–386. doi: 10.1111/j.1439-0426.2011.01733.x CrossRefGoogle Scholar
  8. Clark TD, Sandblom E, Jutfelt F (2013) Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations. J Exp Biol 216(15):2771–2782. doi: 10.1242/jeb.084251 CrossRefPubMedGoogle Scholar
  9. Coughlin DJ (2002) Aerobic muscle function during steady swimming in fish. Fish & Fisheries 3(2):63–78. doi: 10.1046/j.1467-2979.2002.00069.x CrossRefGoogle Scholar
  10. Crocker CE, Cech JJ (1997) Effects of environmental hypoxia on oxygen consumption rate and swimming activity in juvenile white sturgeon, Acipenser transmontanus, in relation to temperature and life intervals. Environ Biol Fish 50(4):383–389. doi: 10.1023/A:1007362018352 CrossRefGoogle Scholar
  11. Deslauriers D, Kieffer JD (2012) The effects of temperature on swimming performance of juvenile shortnose sturgeon (Acipenser brevirostrum). J Appl Ichthyol 28(2):176–181. doi: 10.1111/j.1439-0426.2012.01932.x CrossRefGoogle Scholar
  12. Domenici P (2010) Context-dependent variability in the components of fish escape response: integrating locomotor performance and behavior. Journal of Experiment Zoology Part A - Ecological Genetics and Physiology 313(2):59–79. doi: 10.1002/jez.580 CrossRefGoogle Scholar
  13. Farrell AP (2009) Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids. J Exp Biol 212(23):3771–3780. doi: 10.1242/jeb.023671 CrossRefPubMedGoogle Scholar
  14. Farrell AP, Johansen JA, Steffensen JF, Moyes CD, West TG, Suarez RK (1990) Effects of exercise training and coronary ablation on swimming perform. Can J Zool 68(6):1174–1179CrossRefGoogle Scholar
  15. Farrell AP, Gamperl AK, Birtwell IK (1998) Prolonged swimming, recovery and repeat swimming performance of mature sockeye salmon Oncorhynchus nerka exposed to moderate hypoxia and pentachlorophenol. J Exp Biol 201(14):2183–2193PubMedGoogle Scholar
  16. Feng GP, Zhuang P, Zhang LZ, Duan M, Liu JY (2010) Effects of temperature on oxidative stress biomarkers in juvenile Chinese sturgeon (Acipensersinensis) under laboratory conditions. Adv Mater Res 343-344:497–504. doi: 10.4028/www.scientific.net/AMR.343-344.497 CrossRefGoogle Scholar
  17. Graaf FD, Raamsdonk WV, Hasselbaink H, Diegenbach PC, Mos W, Smit-Onel MJ (1990) Enzyme histochemistry of the spinal cord and the myotomal musculature in the teleost fish Brachydanio rerio. Effects of endurance training and prolonged reduced locomotory activity. Zeitschrift feur mikroskopischanatomische Forschung 104:593–606Google Scholar
  18. Haman F, Zwingelstein G, Weber JM (1997) Effects of hypoxia and low temperature on substrate fluxes in fish: plasma metabolite concentrations are misleading. Am J Physiol 273:2046–2054Google Scholar
  19. Hanna SK, Haukenes AH, Foy RJ, Buck CL (2008) Temperature effects on metabolic rate, swimming performance and condition of Pacific cod Gadus macrocephalus Tilesius. J Fish Biol 72(4):1068–1078. doi: 10.1111/j.1095-8649.2007.01791.x CrossRefGoogle Scholar
  20. He X, Lu S, Liao M, Zhu X, Zhang M, Li S (2013) Effects of age and size on critical swimming speed of juvenile Chinese sturgeon Acipenser sinensis at seasonal temperatures. J Fish Biol 82(3):1047–1056. doi: 10.1111/j.1095-8649.2012.12015.x CrossRefPubMedGoogle Scholar
  21. Holt R E. 2015. Climate change in fish: effects of respiratory constraints on optimal life history and behaviour. Biology Letters, 11.  http://dx.doi.org/10.1098/rsbl.2014.1032
  22. Jain KE, Birtwell IK, Farrell AP (2011) Repeat swimming performance of mature sockeye salmon following a brief recovery period: a proposed measure of fish health and water quality. Can J Zool 76(8):1488–1496. doi: 10.1139/cjz-76-8-1488 CrossRefGoogle Scholar
  23. Jain KE, Farrell AP (2003) Influence of seasonal temperature on the repeat swimming performance of rainbow trout Oncorhynchus mykiss. J Exp Biol 206(20):3569–3579. doi: 10.1242/jeb.00588 CrossRefPubMedGoogle Scholar
  24. Kieffer JD (2000) Review limits to exhaustive exercise in fish. Comparative biochemistry and physiology. A, Molecular & Integrative Physiology 126(2):161–179. doi: 10.1016/S1095-6433(00)00202-6 CrossRefGoogle Scholar
  25. Kieffer JD, Arsenault LM, Litvak MK (2009) Behavior and performance of juvenile shortnose sturgeon Acipenser brevirostrum at different water velocities. J Fish Biol 74:674–682. doi: 10.1111/j.1095-8649.2008.02139.x CrossRefPubMedGoogle Scholar
  26. Kieffer JD, Penny FM, Papadopoulos V (2014) Temperature has a reduced effect on routine metabolic rates of juvenile shortnose sturgeon (Acipenser brevirostrum). Fish Physiology & Biochemistry 40(2):551–559. doi: 10.1007/s10695-013-9865-8 CrossRefGoogle Scholar
  27. Kynard B, Pugh D, Parker T (2011) Passage and behaviour of cultured lake sturgeon in a prototype side-baffle fish ladder: I. Ladder hydraulics and fish ascent. J Appl Ichthyol 27(S):77–88. doi: 10.1111/j.1439-0426.2011.01831.x CrossRefGoogle Scholar
  28. Lee CG, Devlin RH, Farrell AP (2003) Swimming performance, oxygen consumption and excess post-exercise oxygen consumption in adult transgenic and ocean-ranched coho salmon. J Fish Biol 62(4):753–766. doi: 10.1046/j.1095-8649.2003.00057.x CrossRefGoogle Scholar
  29. 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(1):26–32. doi: 10.1242/jeb.032136 CrossRefPubMedGoogle Scholar
  30. Mazloumi N, Johansen JL, Doubleday ZA, Gillanders BM (2017) Q 10 measures of metabolic performance and critical swimming speed in King George whiting Sillaginodes punctatus. J Fish Biol. doi: 10.1111/jfb.13273 PubMedGoogle Scholar
  31. McCue MD (2004) General effects of temperature on animal biology. In temperature dependent sex determination (Valenzuela N & Lance V A, eds), 71–78. Washington D C: Smithsonian BooksGoogle Scholar
  32. Milligan CL (1996) Metabolic recovery from exhaustive exercise in rainbow trout. Comparative Biochemistry and Physiology. A, Physiology 113(1):51–60. doi: 10.1016/0300-9629(95)02060-8
  33. Novinger DC, Coon TG (2000) Behavior and physiology of the redside dace, Clinostomus elongatus, a threatened species in Michigan. Environ Biol Fish 57(3):315–326. doi: 10.1023/A:1007526414384
  34. Palstra AP, Mes D, Kusters K, Roques JA, Flik G, Kloet K (2014) Forced sustained swimming exercise at optimal speed enhances growth of juvenile yellowtail kingfish (Seriola lalandi). Front Physiol 5:506–506. doi: 10.3389/fphys.2014.00506
  35. Pang X, Yuan XZ, Cao ZD, Zhang YG, Fu SJ (2015) The effect of temperature on repeat swimming performance in juvenile qingbo (spinibarbus sinensis). Fish Physiol Biochem 41(1):19–29Google Scholar
  36. Pelicice FM, Pompeu PS, Agostinho AA (2015) Large reservoirs as ecological barriers to downstream movements of neotropical migratory fish. Fish & Fisheries 16(4):697–715. doi: 10.1111/faf.12089 CrossRefGoogle Scholar
  37. Randall D, Brauner C (1991) Effects of environmental factors on exercise in fish. J Exp Biol 160(2):113–126Google Scholar
  38. Sänger AM (1993) Limits to the acclimation of fish muscle. Reviews in Fish Biology & Fisheries 3(1):1–15. doi: 10.1007/BF00043295 CrossRefGoogle Scholar
  39. Urfi AJ, Talesara CL (1989) Response of pectoral adductor muscle of Channa punctata to altered workload. Indian J Exp Biol 27(7):668–669PubMedGoogle Scholar
  40. Wang CY, Du H, Zhang H, Wu JM, Liu ZG, Wei QW (2014) Migration of juvenile and sub-adult Chinese sturgeon Acipenser sinensis Gray, 1835 in the Yangtze River, China below the Gezhouba Dam. J Appl Ichthyol 30(6):1109–1114. doi: 10.1111/jai.12599 CrossRefGoogle Scholar
  41. Warren CE and Davis GE (1967) Laboratory studies on the feeding, bioenergetics, and growth of fish, In The Biological Basis for Freshwater Fish Production (Gerking S, ed.) 175–214. Blackwell, OxfordGoogle Scholar
  42. Webb PW (1993) Swimming. In: Evans DH (ed) The physiology of fishes. CRC Press, Boca Raton, pp 47–73Google Scholar
  43. Xie P, Han X (2003) Three-Gorges Dam: risk to ancient fish. Science 302(5648):1149–1149CrossRefPubMedGoogle Scholar
  44. Yan GJ, He XK, Cao ZD, Fu SJ (2015) Effects of fasting and feeding on the fast-start swimming performance of southern catfish Silurus meridionalis. J Fish Biol 86(2):605–614. doi: 10.1111/jfb.12595 CrossRefGoogle Scholar
  45. Yang DS, Kynard B, Wei Q, Chen X, Zheng WM, Du H (2006) Distribution and movement of Chinese sturgeon, Acipenser sinensis, on the spawning ground located below the Gezhouba Dam during spawning seasons. J Appl Ichthyol 22(S):145–151. doi: 10.1111/j.1439-0426.2007.00943.x CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Xi Yuan
    • 1
    • 2
  • Yi-hong Zhou
    • 2
  • Ying-ping Huang
    • 1
  • Wen-tao Guo
    • 3
  • David Johnson
    • 1
    • 4
  • Qing Jiang
    • 1
  • Jin-jie Jing
    • 1
  • Zhi-ying Tu
    • 1
  1. 1.Engineering Research Center of Eco-environment in Three Gorges Reservoir Region, Ministry of EducationChina Three Gorges UniversityYichangChina
  2. 2.College of Hydraulic & Environmental engineeringChina Three Gorges UniversityYichangChina
  3. 3.Hubei Key Laboratory of Three Gorges Project for Conservation of Fishes, Chinese sturgeon Research InstituteChina Three Gorges CorporationYichangChina
  4. 4.School of Natural Sciences and MathematicsFerrum CollegeFerrumUSA

Personalised recommendations