Temperature Compensation of Aerobic Capacity and Performance in the Antarctic Pteropod, Clione antarctica , Compared with its Northern Congener, C. limacina

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 fre...

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Published in:Journal of Experimental Biology
Main Authors: Dymowska, Agnieszka K., Manfredi, Thomas, Rosenthal, Joshua J. C., Seibel, Brad A.
Format: Article in Journal/Newspaper
Language:unknown
Published: Digital Commons @ University of South Florida 2012
Subjects:
Online Access:https://digitalcommons.usf.edu/msc_facpub/2360
https://doi.org/10.1242/jeb.070607
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spelling ftunisfloridatam:oai:digitalcommons.usf.edu:msc_facpub-3388 2023-05-15T13:35:22+02:00 Temperature Compensation of Aerobic Capacity and Performance in the Antarctic Pteropod, Clione antarctica , Compared with its Northern Congener, C. limacina Dymowska, Agnieszka K. Manfredi, Thomas Rosenthal, Joshua J. C. Seibel, Brad A. 2012-01-01T08:00:00Z https://digitalcommons.usf.edu/msc_facpub/2360 https://doi.org/10.1242/jeb.070607 unknown Digital Commons @ University of South Florida https://digitalcommons.usf.edu/msc_facpub/2360 https://doi.org/10.1242/jeb.070607 Marine Science Faculty Publications mitochondria cristae citrate synthase cold temperature Antarctica Life Sciences article 2012 ftunisfloridatam https://doi.org/10.1242/jeb.070607 2022-04-07T17:43:38Z 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. Article in Journal/Newspaper Antarc* Antarctic Antarctica Arctic Clione limacina North Atlantic Southern Ocean Digital Commons University of South Florida (USF) Arctic Antarctic Southern Ocean The Antarctic Journal of Experimental Biology
institution Open Polar
collection Digital Commons University of South Florida (USF)
op_collection_id ftunisfloridatam
language unknown
topic mitochondria
cristae
citrate synthase
cold
temperature
Antarctica
Life Sciences
spellingShingle mitochondria
cristae
citrate synthase
cold
temperature
Antarctica
Life Sciences
Dymowska, Agnieszka K.
Manfredi, Thomas
Rosenthal, Joshua J. C.
Seibel, Brad A.
Temperature Compensation of Aerobic Capacity and Performance in the Antarctic Pteropod, Clione antarctica , Compared with its Northern Congener, C. limacina
topic_facet mitochondria
cristae
citrate synthase
cold
temperature
Antarctica
Life Sciences
description 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.
format Article in Journal/Newspaper
author Dymowska, Agnieszka K.
Manfredi, Thomas
Rosenthal, Joshua J. C.
Seibel, Brad A.
author_facet Dymowska, Agnieszka K.
Manfredi, Thomas
Rosenthal, Joshua J. C.
Seibel, Brad A.
author_sort Dymowska, Agnieszka K.
title Temperature Compensation of Aerobic Capacity and Performance in the Antarctic Pteropod, Clione antarctica , Compared with its Northern Congener, C. limacina
title_short Temperature Compensation of Aerobic Capacity and Performance in the Antarctic Pteropod, Clione antarctica , Compared with its Northern Congener, C. limacina
title_full Temperature Compensation of Aerobic Capacity and Performance in the Antarctic Pteropod, Clione antarctica , Compared with its Northern Congener, C. limacina
title_fullStr Temperature Compensation of Aerobic Capacity and Performance in the Antarctic Pteropod, Clione antarctica , Compared with its Northern Congener, C. limacina
title_full_unstemmed Temperature Compensation of Aerobic Capacity and Performance in the Antarctic Pteropod, Clione antarctica , Compared with its Northern Congener, C. limacina
title_sort temperature compensation of aerobic capacity and performance in the antarctic pteropod, clione antarctica , compared with its northern congener, c. limacina
publisher Digital Commons @ University of South Florida
publishDate 2012
url https://digitalcommons.usf.edu/msc_facpub/2360
https://doi.org/10.1242/jeb.070607
geographic Arctic
Antarctic
Southern Ocean
The Antarctic
geographic_facet Arctic
Antarctic
Southern Ocean
The Antarctic
genre Antarc*
Antarctic
Antarctica
Arctic
Clione limacina
North Atlantic
Southern Ocean
genre_facet Antarc*
Antarctic
Antarctica
Arctic
Clione limacina
North Atlantic
Southern Ocean
op_source Marine Science Faculty Publications
op_relation https://digitalcommons.usf.edu/msc_facpub/2360
https://doi.org/10.1242/jeb.070607
op_doi https://doi.org/10.1242/jeb.070607
container_title Journal of Experimental Biology
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