Temperature compensation of aerobic capacity and performance in the Antarctic pteropod,Clione antarctica, compared to its northern congener,C. limacina

Abstract

SUMMARYIn 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±1.3m ). The values for cold-adapted populations are on par with those found in highperformance 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 speciesʼ respective temperature. The elevated capacity in the wing muscles is reflected in the partial compensation of whole-animal oxygen consumption and feeding rates.

Is metabolic rate a universal ‘pacemaker’ for biological processes?

“…They may adaptively adjust their activities to temperature changes in ways that are not predicted by simple Boltzmann-Arrhenius kinetics. These and other examples of temperature compensation (Clarke, 2004(Clarke, , 2006O'Connor et al, 2007;Terblanche et al, 2009;Hare et al, 2010;White, Alton & Frappell, 2011;Dymowska et al, 2012;Pyl et al, 2012) suggest that even when the rates of biological processes increase with increasing temperature as predicted by the MTE, biological systems may be actively permitting (rather than merely passively succumbing to) such responses, at least to some extent, because they increase the rates of fitness-related processes (e.g. Furthermore, temperature influences the locomotor activity of this snail in a markedly different way than its metabolic rate , which also contradicts the metabolic pacemaker view (also see Section III for citations of other examples of temperature-induced dissociations between metabolic rate and the rates of other biological processes).…”

Energetic Effects of Pre-hatch Albumen Removal on Embryonic Development and Early Ontogeny in Gallus gallus

“…However, at the time of hatching, most of the albumen had already been consumed, thus successful hatching is more likely a factor of the physiological effect of removal of the albumen, for example changes in enzyme activity of skeletal muscles, than physical disturbance per-se . We therefore propose a potential explanation for differential hatching success, considering that the enzymatic activity of CS and COX in skeletal muscle (see Figure 4) are considered indicators of locomotors capacities in many taxa (Kohlsdorf et al, 2004; Dymowska et al, 2012). However, while we cannot discard that glycolysis-driven energy generation may be important for these processes, the fiber types present in legs (mainly responsible for hatching) are those characterized predominantly by oxidative metabolism (Ono et al, 1993), which suggests a causal effect: the reduction of oxidative activity in skeletal muscles, especially in legs, explains the reduction in the capacities of breaking and leaving the egg shell, hence reducing the survival of chicks.…”

Slow swimming, fast strikes: effects of feeding behavior on scaling of anaerobic metabolism in epipelagic squid

“…Seibel (Seibel, 2007) reported an even shallower scaling slope for citrate synthase in active squids (b=-0.1), including D. gigas and other ommastrephids. As with ODH, the increased citrate synthase activity with size (relative to fishes) could be achieved via more or 'better' mitochondria or via increased red muscle mass (Dymowska et al, 2012). The latter possibility would displace white muscle tissue at larger sizes, which could play a role in the negative scaling coefficient for ODH in D. gigas.…”

“…However, displacing white muscle is not without costs. For example, the Antarctic pteropod mollusk Clione antarctica elevates red muscle mass in locomotory muscles as compensation for cold temperature but at the expense of burst locomotory capacity (Dymowska et al, 2012;Rosenthal et al, 2009). Evidence suggests that the ratio of mitochondria-rich to mitochondria-poor muscle fibers does not change appreciably with size after an initial growth period in several species of squid (Moltschaniwskyj, 1994;Pecl and Moltschaniwskyj, 1997;Preuss et al, 1997).…”