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The Journal of Experimental Biology 206, 411-421 (2003)
doi: 10.1242/jeb.00088

Muscle fine structure may maintain the function of oxidative fibres in haemoglobinless Antarctic fishes

K. M. O'Brien^1,*, C. Skilbeck², B. D. Sidell¹ and S. Egginton^2,

¹ School of Marine Sciences, University of Maine, Orono, ME 04469, USA
² Department of Physiology, University of Birmingham, B15 2TT, UK
^* Present address: Department of Molecular, Cellular and Developmental Biology, University of Colorado at Boulder, Boulder, CO 80309, USA

Author for correspondence (e-mail: s.egginton{at}bham.ac.uk)

Accepted 21 October 2002

Muscle fine structure and metabolism were examined in four species of Antarctic fishes that vary in their expression of haemoglobin (Hb). To determine how locomotory pectoral muscles maintain function, metabolic capacity, capillary supply and fibre ultrastructure were examined in two nototheniid species that express Hb (Notothenia coriiceps and Gobionotothen gibberifrons) and two species of channichthyid icefish that lack Hb (Chaenocephalus aceratus and Chionodraco rastrospinosus). Surprisingly, icefish have higher densities of mitochondria than red-blooded species (C. aceratus, 53±3% of cell volume; C. rastrospinosus, 39±3%; N. coriiceps, 29±3%; G. gibberifrons, 25±1%). Despite higher mitochondrial densities the aerobic metabolic capacities per g wet mass, estimated from measurements of maximal activities of key metabolic enzymes, are lower in icefish compared to red-blooded species. This apparent incongruity can be explained by the significantly lower mitochondrial cristae surface area per unit mitochondrion volume in icefishes (C. aceratus, 20.8±1.6 µm^-1; C. rastrospinosus, 25.5±1.8 µm^-1) compared to red-blooded species (N. coriiceps, 33.6±3.0 µm^-1; G. gibberifrons, 37.7±3.6 µm^-1). Consequently, the cristae surface area per unit muscle mass is conserved at approximately 9 m²g^-1. Although high mitochondrial densities in icefish muscle do not enhance aerobic metabolic capacity, they may facilitate intracellular oxygen movement because oxygen is more soluble in lipid, including the hydrocarbon core of intracellular membrane systems, than in aqueous cytoplasm. This may be particularly vital in icefish, which have larger oxidative muscle fibres compared to red-blooded nototheniods (C. aceratus, 2932±428 µm²; C. rastrospinosus, 9352±318 µm²; N. coriiceps, 1843±312 µm²; G. gibberifrons, 2103±194 µm²). These large fibres contribute to a relatively low capillary density, which is partially compensated for in icefish by a high index of tortuosity in the capillary bed (C. aceratus=1.4, N. coriiceps=1.1).

Key words: muscle, haemoglobin, Antarctic icefish, capillary supply, metabolic enzyme, lipid, mitochondria

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