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The Journal of Experimental Biology 205, 769-779 (2002)
© 2002 The Company of Biologists Limited

Peripheral oxygen transport in skeletal muscle of Antarctic and sub-Antarctic notothenioid fish

S. Egginton^1,*, C. Skilbeck¹, L. Hoofd², J. Calvo³ and I. A. Johnston⁴

¹ Department of Physiology, University of Birmingham, Birmingham B15 2TT, UK,
² Department of Physiology, University of Nijmegen, 6525 Nijmegen, The Netherlands,
³ CONICET, CADIC, Ushuaia, Argentina and
⁴ School of Biology, Gatty Marine Laboratory, University of St Andrews, Fife KY16 8LB, Scotland

*e-mail: s.egginton{at}bham.ac.uk

Accepted 7 January 2002

Transcellular oxygen flux was modelled mathematically in the aerobic skeletal muscles of perciform fish species living at widely different temperatures (Antarctica, sub-Antarctica and the Mediterranean Sea). Using structural data derived from stereological analysis of electron micrographs, mean fibre P_O2 was calculated on the basis of temperature-corrected rates of mitochondrial respiration and oxygen diffusion. The mean muscle fibre diameter (MFD) among Antarctic notothenioids was in the range 17–61 µm and mitochondrial volume density, Vv(mit,f), was 0.27–0.53, but capillary-to-fibre ratio varied only between 1.2 and 1.5. For a mean capillary P_O2 of 6 kPa, the model predicted a mean tissue P_O2 in the range 0.7–5.8 kPa at the estimated maximum aerobic capacity (_O2max). The lowest levels of tissue oxygenation were found in the pectoral muscle fibres of the icefish Chaenocephalus aceratus, which lacks the respiratory pigments haemoglobin and myoglobin. Red-blooded notothenioids found in the sub-Antarctic had a similar muscle fine structure to those caught south of the Antarctic Convergence, with an MFD of 20–41 µm and Vv(mit,f) of 0.27–0.33, resulting in an estimated mean P_O2 of 4–5 kPa at _O2max. Mean tissue P_O2 in the sub-Antarctic icefish Champsocephalus esox, with greater MFD and Vv(mit,f), 56 µm and 0.51, respectively, was calculated to exceed 1 kPa at winter temperatures (4°C), although oxidative metabolism was predicted to be impaired at the summer maximum of 10°C. At the high end of the thermal range, related perciform species from the Mediterranean had a negligible drop in intracellular P_O2 across their small-diameter fibres, to a minimum of 5.4 kPa, comparable with that predicted for Trematomus newnesi from the Antarctic (5.6 kPa) with a similar MFD. These data suggest that, within a single phylogenetic group, integrative structural adaptations potentially enable a similar degree of tissue oxygenation over a 20°C range of environmental temperature in the red-blooded notothenioids, and that this is compromised by the lack of respiratory pigments in the icefishes. The mean capillary radius was 1.5 times greater in the two icefish than in the other notothenioids, and the model simulations indicate that the evolution of wide-bore capillaries is essential to maintain tissue oxygenation in the absence of respiratory pigments.

Key words: diffusion, icefish, mathematical model, oxygen tension, stereology, notothenioid fish.

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