Abstract
In ectotherms living in cold waters, locomotory performance is constrained by a slower generation of the ATP that is needed to fuel muscle contraction. Both polar and temperate pteropods of the genus Clione, however, are able to swim continuously by flapping their parapodia (wings) at comparable frequencies at their respective habitat temperatures. Therefore, we expected polar species to have increased aerobic capacities in their wing muscles when measured at common temperatures. We investigated muscle and mitochondrial ultrastructure of Clione antarctica from the Southern Ocean (-1.8°C) and populations of a sister species, Clione limacina, from the Arctic (-0.5 to 3°C) and from the North Atlantic (10°C). We also measured oxygen consumption and the activity of the mitochondrial enzyme citrate synthase (CS) in isolated wings of the two species. The Antarctic species showed a substantial up-regulation of the density of oxidative muscle fibers, but at the expense of fast-twitch muscle fibers. Mitochondrial capacity was also substantially increased in the Antarctic species, with the cristae surface density (58.2±1.3μm(2)μm(-3)) more than twice that found in temperate species (34.3±0.8μm(2)μm(-3)). Arctic C. limacina was intermediate between these two populations (43.7±0.5μm(2)μm(-3)). The values for cold-adapted populations are on par with those found in high-performance vertebrates. As a result of oxidative muscle proliferation, CS activity was 4-fold greater in C. antarctica wings than in temperate C. limacina when measured at a common temperature (20°C). Oxygen consumption of isolated wing preparations was comparable in the two species when measured at their respective habitat temperatures. These findings indicate complete compensation of ATP generation in wing muscles across a 10°C temperature range, which supports similar wing-beat frequencies during locomotion at each species' respective temperature. The elevated capacity in the wing muscles is reflected in the partial compensation of whole-animal oxygen consumption and feeding rates.
Highlights
In ectotherms inhabiting cold waters, rates of substrate diffusion and enzymatic activity are constrained by the low temperature
Fourweek exposure of C. limacina to 0°C in the laboratory, as well as seasonal acclimation to cold temperature in the wild, did not result in proliferation of oxidative muscle fibers in the muscle bundles (Fig. 1). This is in contrast to C. antarctica, chronically exposed to the cold (–1.86°C), which have muscle bundles composed entirely of mitochondria-rich muscle fibers (Rosenthal et al, 2009)
In Arctic C. limacina, adaptation to cold is apparent in an increase in cristae surface densities; while in C. antarctica, compensation for cold is achieved by both the proliferation of oxidative muscle fibers (Rosenthal et al, 2009) and higher cristae surface densities
Summary
In ectotherms inhabiting cold waters, rates of substrate diffusion and enzymatic activity are constrained by the low temperature (for a review, see Guderley and St-Pierre, 2002). Fish and some invertebrates exposed to seasonal or latitudinal reductions in temperature show proliferation of aerobic muscle fibers (Sidell, 1980; Johnston and Maitland, 1980; Tyler and Sidell, 1984) as well as an enhanced metabolic capacity of those fibers via (1) elevated mitochondrial densities (Johnston et al, 1998; Sommer and Pörtner, 2002), (2) increased surface density of folded membranes inside a mitochondrion (cristae) (St-Pierre et al, 1998; Kilarski et al, 1996) and/or (3) mitochondrial enzymatic capacities (Crockett and Sidell, 1990; Kawall et al, 2002) Such modifications presumably enhance aerobic capacity because mitochondria are the primary site of aerobic ATP production. Mitochondria may facilitate intracellular oxygen diffusion, which is constrained in cold water (Sidell, 1998)
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