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Reduced and reversed temperature dependence of blood oxygenation in an ectothermic scombrid fish: implications for the evolution of regional heterothermy?

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Abstract

Tunas (family Scombridae) are exceptional among most teleost fishes in that they possess vascular heat exchangers which allow heat retention in specific regions of the body (termed ‘regional heterothermy’). Seemingly exclusive to heterothermic fishes is a markedly reduced temperature dependence of blood–oxygen (blood–O2) binding, or even a reversed temperature dependence where increasing temperature increases blood–O2 affinity. These unusual binding properties have been documented in whole blood and in haemoglobin (Hb) solutions, and they are hypothesised to prevent oxygen loss from arteries to veins within the vascular heat exchangers and/or to prevent excessive oxygen unloading to the warm tissues and ensure an adequate supply of oxygen to tissues positioned efferent to the heat exchangers. The temperature sensitivity of blood–O2 binding has not been characterised in an ectothermic scombrid (mackerels and bonitos), but the existence of the unusual binding properties in these fishes would have clear implications for their proposed association with regional heterothermy. Accordingly, the present study examined oxygenation of whole blood of the chub mackerel (Scomber japonicus) at 10, 20 and 30°C and at 0.5, 1 and 2% CO2. Oxygen affinity was generally highest at 20°C for all levels of CO2. Temperature-independent binding was observed at low (0.5%) CO2, where the PO2 at 50% blood–O2 saturation (P 50) was not statistically different at 10 and 30°C (2.58 vs. 2.78 kPa, respectively) with an apparent heat of oxygenation (∆H°) close to zero (−6 kJ mol−1). The most significant temperature-mediated difference occurred at high (2%) CO2, where the P 50 at 10°C was twofold higher than that at 20°C with a corresponding ∆H° of +43 kJ mol−1. These results provide clear evidence of independent and reversed open-system temperature effects on blood oxygenation in S. japonicus, and it is therefore speculated that these unusual blood–O2 binding characteristics may have preceded the evolution of vascular heat exchangers and regional heterothermy in fishes.

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Acknowledgments

All field collections were conducted under the California Department of Fish and Game Scientific Collection Permit SCP-2471, the Pfleger Institute of Environmental Research Animal Care Protocol (#138-145-08), and the Animal Care and Use Committee of the University of Massachusetts, Dartmouth (#05-06). T. D. Clark was supported by a Killam Postdoctoral Fellowship. The research was supported by Natural Sciences and Engineering Research Council of Canada Discovery Grants to A. P. Farrell and C. J. Brauner. We thank Michael Berenbrink and David Randall for discussions relating to this work and for highlighting some important publications.

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Authors and Affiliations

  1. Faculty of Land and Food Systems, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

    Timothy Darren Clark & A. P. Farrell

  2. Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

    J. L. Rummer, A. P. Farrell & C. J. Brauner

  3. Pfleger Institute of Environmental Research, Oceanside, CA, 92054, USA

    C. A. Sepulveda

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  1. Timothy Darren Clark
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  2. J. L. Rummer
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  3. C. A. Sepulveda
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  4. A. P. Farrell
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  5. C. J. Brauner
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Correspondence to Timothy Darren Clark.

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Communicated by I. D. Hume.

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Clark, T.D., Rummer, J.L., Sepulveda, C.A. et al. Reduced and reversed temperature dependence of blood oxygenation in an ectothermic scombrid fish: implications for the evolution of regional heterothermy?. J Comp Physiol B 180, 73–82 (2010). https://doi.org/10.1007/s00360-009-0388-7

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  • DOI: https://doi.org/10.1007/s00360-009-0388-7

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