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The effects of dissolved oxygen levels on the metabolic interaction between digestion and locomotion in Cyprinid fishes with different locomotive and digestive performances

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Abstract

To test whether the effects of water oxygen concentration ([O2]) on the metabolic interaction between locomotion and digestion differ between fish species with different locomotive and digestive behaviours in normoxia, we investigated the swimming performance of fasted and fed fish at water [O2] of 1, 2 and 8 (normoxia) mg L−1 (2.5, 5 and 20 kPa) at 25°C in three juvenile Cyprinidae fish species: goldfish (Carassius auratus), common carp (Cyprinus carpio) and qingbo (Spinibarbus sinensis). Digestion, taxon and water [O2] all had significant effects on the pre-exercise oxygen consumption rate \( (\dot{M}{\text{O}}_{{ 2 {\text{pre-exercise}}}} ) \) and the swimming performance (P < 0.05). Among the three fishes, qingbo showed the highest swimming performance and the lowest feeding \( \dot{M}{\text{O}}_{2} \) at the saturated water [O2], and its active oxygen consumption rate \( (\dot{M}{\text{O}}_{{ 2 {\text{active}}}} ) \) and critical swimming speed (U crit) decreased the most with decreases in water [O2]. Qingbo exhibited a locomotion-priority metabolic mode at all three water [O2]. Digestion was sacrificed to locomotion in a postprandial swimming situation, but fed qingbo could not maintain their U crit at water [O2] of 2 and 1 mg L−1. Goldfish showed the lowest swimming performance and the highest feeding \( \dot{M}{\text{O}}_{2} \) at the saturated water [O2]. They exhibited a digestion-priority metabolic mode at high water [O2]. However, with a decrease in water [O2], the feeding \( \dot{M}{\text{O}}_{2} \) decreased more acutely than the respiratory capacity; thus, digestion and locomotion performed independently in a postprandial swimming situation (i.e., an additive metabolic mode) at a water [O2] of 1 mg L−1. The common carp showed moderate and balanced swimming performance and feeding \( \dot{M}{\text{O}}_{2} \) at the saturated water [O2], and exhibited an additive metabolic mode at all 3 water [O2], because digestion, swimming and respiratory capacities decreased in parallel with the decrease in water [O2].

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References

  • Alsop DH, Wood CM (1997) The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout (Oncorhynchus mykiss). J Exp Biol 200:2337–2346

    PubMed  Google Scholar 

  • Altimiras J, Claireaux G, Sandblom E, Farrell AP, McKenzie DJ, Axelsson M (2008) Gastrointestinal blood flow and postprandial metabolism in swimming sea bass Dicentrarchus labrax. Physiol Biochem Zool 81:663–672

    Article  PubMed  Google Scholar 

  • Andersen JB, Wang T (2003) Cardiorespiratory effects of forced activity and digestion in toads. Physiol Biochem Zool 76:459–470

    Article  PubMed  Google Scholar 

  • Bell WH, Terhune LDB (1970) Water tunnel design for fisheries research. Fish Res Board Can Tech Rep 195:1–69

    Google Scholar 

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

    Article  Google Scholar 

  • Duan XB, Chen DQ, Liu SP, Chi CG, Yang RH (2002) Studies on status of fishery resources in Three Gorges reservoir reaches of the Yangtze River. Acta Hydrobiol Sin 26:605–611

    Google Scholar 

  • Dupont-Prinet A, Claireaux G, McKenzie DJ (2009) Effects of feeding and hypoxia on cardiac performance and gastro-intestinal blood flow during critical speed swimming in the sea bass Dicentrarchus labrax. Comp Biochem Physiol 154A:233–240

    CAS  Google Scholar 

  • Fitzgibbon QP, Srawbridge A, Seymour RS (2007) Metabolic scope, swimming performance and the effects of hypoxia in the mulloway, Argyrosomus japonicus (Pisces: Sciaenidae). Aquaculture 270:358–368

    Article  Google Scholar 

  • Fu SJ, Zeng LQ, Li XM, Pang X, Cao ZD, Peng JL, Wang YX (2009) The behavioral, digestive and metabolic characteristics of fishes with different foraging strategies. J Exp Biol 212:2296–2302

    Article  PubMed  Google Scholar 

  • Fu SJ, Li XM, Zhao WW, Peng JL, Pang X, Cao ZD (2010) The locomotive and metabolic strategies of goldfish under different dissolved oxygen level. J Chongqing Norm Univ (Nat Sci) 57:14–18

    Google Scholar 

  • Fu SJ, Brauner CJ, Cao ZD, Richards JG, Peng JL, Dhillon R, Wang YX (2011a) 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  PubMed  CAS  Google Scholar 

  • Fu SJ, Pang X, Cao ZD, Peng JL, Yan GJ (2011b) The effects of fasted on the metabolic interaction between digestion and locomotion in juvenile southern catfish (Silurus meridionalis Chen). Comp Biochem Physiol 158A:498–505

    CAS  Google Scholar 

  • Furnell DJ (1987) Partitioning of locomotor and feeding metabolism in sablefish (Anoplopoma fimbria). Can J Zool 65:486–489

    Article  Google Scholar 

  • Hicks JWH, Bennett AF (2004) Eat and run: prioritization of oxygen delivery during elevated metabolic states. Res Physiol Neurol 144:215–224

    Article  Google Scholar 

  • Jourdan-Pineau H, Dupont-Prinet A, Claireaux G, McKenzie DJ (2010) An investigation of metabolic prioritization in the European sea bass, Dicentrarchus labrax. Physiol Biochem Zool 83:68–77

    Article  PubMed  Google Scholar 

  • Kong XH, Wang XZ, Gan XN, Li JB, He SP (2007) Phylogenetic relationships of Cyprinidae (Teleostei: Cypriniformes) inferred from the partial S6K1 gene sequences and implication of indel sites in intron 1. Sci China Ser 50C:780–788

    Google Scholar 

  • Lee CG, Farrell AP, Lotto A, MacNctt 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  PubMed  CAS  Google Scholar 

  • Li XM, Cao ZD, Fu SJ (2010a) The effect of exercise training on the metabolic interaction between digestion and locomotion in juvenile southern catfish (Silurus meridionalis). J Exp Zool 313A:557–563

    Article  Google Scholar 

  • Li XM, Cao ZD, Fu SJ, Peng JL (2010b) The effect of exercise training on the metabolic interaction between digestion and locomotion in juvenile darkbarbel catfish (Peltebngrus vachelli). Comp Biochem Physiol 156A:67–73

    CAS  Google Scholar 

  • Mitrovic D, Dymowska A, Nilsson GE, Perry SF (2009) Physiological consequences of gill remodeling in goldfish (Carassius auratus) during exposure to long-term hypoxia. Am J Physiol 297R:224–234

    Google Scholar 

  • Ott ME, Heisler N, Ultsch GR (1980) A re-evaluation of the relationship between temperature and the critical oxygen tension in freshwater fishes. Comp Biochem Physiol 67A:337–340

    Article  Google Scholar 

  • Pang X, Cao ZD, Peng JL, Fu SJ (2010) The effects of feeding on the swimming performance and metabolic response of juvenile southern catfish, Silurus meridionalis, acclimated at different temperatures. Comp Biochem Physiol 155A:253–258

    CAS  Google Scholar 

  • Pang X, Cao ZD, Peng JL, 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 159A:253–260

    CAS  Google Scholar 

  • Petersen LH, Gamperl AK (2010) Effect of acute and chronic hypoxia on the swimming performance, metabolic capacity and cardiac function of Atlantic cod (Gadus morhua). J Exp Biol 213:808–819

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Seibel BA (2011) Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones. J Exp Biol 214:326–336

    Article  PubMed  CAS  Google Scholar 

  • Sollid J, Weber RE, Nilsson GE (2005) Temperature alters the respiratory surface area of crucian carp Carassius carassius and goldfish Carassius auratus. J Exp Biol 208:1109–1116

    Article  PubMed  Google Scholar 

  • Thorarensen H, Farrell AP (2006) Postprandial intestinal blood flow, metabolic rate, and exercise in Chinook salmon (Oncorhynchus tshawytscha). Physiol Biochem Zool 79:688–694

    Article  PubMed  Google Scholar 

  • Willson JD, Hopkins WA (2011) Prey morphology constrains the feeding ecology of an aquatic generalist predator. Ecology 92:744–754

    Article  PubMed  Google Scholar 

  • 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 157A:212–219

    CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by Grants from the National Science Foundation of China (NSFC 31172096; 30700087), the Natural Science Foundation Project of CQ (CSTC2010BB1089) and the Project of Chongqing Science and Technology Commission (No. CSTC, 2010CA1010) granted to S.J.F. We declare that the experiments comply with the current laws of the country in which the experiments were performed.

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Correspondence to Shi-Jian Fu.

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Communicated by G. Heldmaier.

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Zhang, W., Cao, ZD. & Fu, SJ. The effects of dissolved oxygen levels on the metabolic interaction between digestion and locomotion in Cyprinid fishes with different locomotive and digestive performances. J Comp Physiol B 182, 641–650 (2012). https://doi.org/10.1007/s00360-012-0644-0

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  • DOI: https://doi.org/10.1007/s00360-012-0644-0

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