Ultrastructural design of anuran muscles used for call production in relation to the thermal environment of a species

SJ Ressel
Department of Ecology and Evolutionary Biology, U-43, University of Connecticut, Storrs, CT 06269-3043, USA. sjr@ecology.coa.edu

I examined the aerobic trunk muscles, which are used for call production, of male frogs from species that breed in different thermal environments to test the hypothesis that cold-adapted frogs should have fewer capillaries per unit mitochondrial volume in oxidative muscles than warm-adapted frogs because of reduced mitochondrial function at low temperatures. The species of interest were the cold-temperate Pseudacris crucifer and the warm-tropical Hyla microcephala in the family Hylidae, and the cold-temperate Rana sylvatica and the warm-temperate Rana clamitans in the family Ranidae. Trunk-muscle mitochondrial volume, V(V)(mt,f), was proportionally higher in species with higher mean calling rates (number of notes per hour), irrespective of the familial affinity of a species and the thermal environment in which it vocalized. Trunk-muscle capillary length density, J(V)(c,f), was significantly lower in P. crucifer than in H. microcephala because of significantly higher mean fiber area, a-(f). Conversely, trunk-muscle J(V)(c,f) was similar in the two ranid species. Using total capillary length, J(c), and total mitochondrial volume, V(mt,m), as a measure of maximal oxygen supply and demand, respectively, in trunk muscles, J(c)-to-V(mt,m) ratios were significantly lower in cold-adapted P. crucifer (4.3 km cm(-)(3)) and R. sylvatica (4.8 km cm(-)(3)) than in warm-adapted H. microcephala (7.1 km cm(-)(3)) and R. clamitans (6.4 km cm(-)(3)). In contrast, J(c)-to-V(mt,m) ratios in the more anaerobic gastrocnemius muscle of these species was not related to the thermal environment of a species, which may reflect capillaries conforming to microcirculatory functions, e.g. lactate removal, that take precedence over oxygen delivery. Mitochondrial cristae surface area, S(V)(im,mt), in P. crucifer trunk and gastrocnemius muscles (37.7+/-1.6 and 35.9+/-1.5 m(2 )cm(-)(3) respectively) was, on average, similar to mammalian values, suggesting equivalent structural capacities of muscle mitochondria in these two taxa. Taken together, the present data suggest that trunk-muscle respiratory design may reflect a capillary supply commensurate with maximal levels of oxygen delivery set by mitochondria operating at different environmental temperatures. P. crucifer and H. microcephala trunk muscles were also characterized by a high lipid content, which contrasted with a near absence of trunk-muscle lipids in R. sylvatica and R. clamitans. The extraordinarily high lipid content of P. crucifer trunk muscles (26 % of muscle volume) may serve as an auxiliary oxygen pathway to mitochondria and thus compensate in part for this tissue's reduced capillary/fiber interface. The effect of potentially high depletion rates of trunk-muscle lipid stores on metabolic rates of male frogs while calling is discussed.

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Ultrastructural design of anuran muscles used for call production in relation to the thermal environment of a species