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

Authors

Agnieszka K. Dymowska, University of Rhode Island
Thomas Manfredi, University of Rhode Island
Joshua J. C. Rosenthal
Brad A. Seibel, University of Rhode IslandFollow

Document Type

Article

Date of Original Version

2012

Department

Biological Sciences

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±1.3μm²μm⁻³) more than twice that found in temperate species (34.3±0.8μm²μm⁻³). Arctic C. limacina was intermediate between these two populations (43.7±0.5μm²μm⁻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.

Citation/Publisher Attribution

Dymowska, A. K., Manfredi, T., Rosenthal, J. J.C., & Seibel, B. A. (2012). Temperature compensation of aerobic capacity and performance in the Antarctic pteropod, Clione antarctica, compared with its northern congener, C. limacina. Journal of Experimental Biology, 215, 3370-3378. doi: 10.1242/jeb.070607

Available at: http://dx.doi.org/10.1242/jeb.070607

Comment

Thomas Manfredi is a member of the Department of Kinesiology.