Domestication compromises athleticism and respiratory plasticity in response to aerobic exercise training in Atlantic salmon (Salmo salar)

Commercially selective breeding of Atlantic salmon (Salmo salar) primarily for rapid growth may compromise cardiorespiratory robustness and its related phenotypes. Therefore, a suite of respiratory indices was used to evaluate aerobic capacity and hypoxia tolerance to test the hypothesis that exerci...

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Published in:Aquaculture
Main Authors: Zhang, Yangfan, Timmerhaus, Gerrit, Anttila, Katja, Mauduit, Florian, Jorgensen, Sven Martin, Kristensen, Torstein, Claireaux, Guy, Takle, Harald, Farrell, Anthony P.
Format: Article in Journal/Newspaper
Language:English
Published: Elsevier Science Bv 2016
Subjects:
Online Access:https://archimer.ifremer.fr/doc/00334/44518/44214.pdf
https://doi.org/10.1016/j.aquaculture.2016.05.015
https://archimer.ifremer.fr/doc/00334/44518/
id ftarchimer:oai:archimer.ifremer.fr:44518
record_format openpolar
institution Open Polar
collection Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer)
op_collection_id ftarchimer
language English
topic Athletic robustness
Atlantic salmon
Domestication
Exercise training
Hypoxia tolerance
Respiratory performance
spellingShingle Athletic robustness
Atlantic salmon
Domestication
Exercise training
Hypoxia tolerance
Respiratory performance
Zhang, Yangfan
Timmerhaus, Gerrit
Anttila, Katja
Mauduit, Florian
Jorgensen, Sven Martin
Kristensen, Torstein
Claireaux, Guy
Takle, Harald
Farrell, Anthony P.
Domestication compromises athleticism and respiratory plasticity in response to aerobic exercise training in Atlantic salmon (Salmo salar)
topic_facet Athletic robustness
Atlantic salmon
Domestication
Exercise training
Hypoxia tolerance
Respiratory performance
description Commercially selective breeding of Atlantic salmon (Salmo salar) primarily for rapid growth may compromise cardiorespiratory robustness and its related phenotypes. Therefore, a suite of respiratory indices was used to evaluate aerobic capacity and hypoxia tolerance to test the hypothesis that exercise training can improve the athletic robustness in both domesticated and wild strains of Atlantic salmon, but with the domesticated strain having a less cardiorespiratory plasticity and a lower athletic robustness than the wild strain. We also tested a second hypothesis that a constant acceleration screening protocol should segregate fish according to athletic robustness based on their swimming ability. These hypotheses were tested with parr from Bolaks (domesticated) and Lærdal (wild) strains of Atlantic salmon that were reared under identical hatchery conditions. After screening into either inferior (bottom 20%) or superior (top 20%) swimmers, the four groups of fish (two strains and two swimming performance levels) either were given an 18-day exercise-training regime (an incremental water current of 2.0–2.8 fork lengths s− 1), or were maintained at the control water current (0.5 fork lengths s− 1) for 18 days. Subsequently, fish were sampled for metabolic enzyme analysis in red and white swimming muscles (citrate synthase, CS, and lactate dehydrogenase, LDH; n = 15 from each group) and their individual respiratory capacities were comprehensively assessed by measuring the standard metabolic rate (SMR), maximum rate of oxygen uptake (ṀO2max), absolute aerobic scope (AAS), factorial aerobic scope (FAS), excess post-exercise oxygen consumption (EPOC), critical oxygen level (O2crit) and incipient lethal oxygen saturation (ILOS). Contrary to our expectations, the inferior and superior swimmers were indistinguishable in either strain and these data were pooled. While exercise training produced several tangible benefits for the wild fish, it produced very few for the domesticated fish. For example, the wild strain, but not the domesticated strain, had a significantly higher ṀO2max, AAS and EPOC as a result of training. Also, CS activity in red muscle increased after training to a larger extent in the wild strain than in the domesticated strain. When compared with the wild strain, the domesticated strain had a significantly lower ṀO2max, AAS, FAS and CS activity in white muscle. Thus, the domesticated strain appeared to be athletically less robust than the wild strain. These results imply that approximately ten generations of selective breeding for rapid growth in commercial aquaculture have reduced the overall athletic robustness of domesticated salmon as compared to their wild conspecifics, and given the success in improving athletic robustness of the wild strain, it still remains to be seen whether an exercise training protocol can be developed that will provide benefits to the salmon aquaculture industry. Statement of relevance This manuscript fits perfectly with the scope of aquaculture. We address the possibility that the Norwegian Atlantic salmon (Salmo salar) breeding program that extensively focuses on commercial benefits traits may be compromising the cardiorespiratory system, which may contribute to the mortality of smolts after seawater transfer. We hypothesized that a combination of exercise-screening and exercise-training protocols could select for superior cardiorespiratory performance. This hypothesis was tested by comparing domesticated and wild Norwegian Atlantic salmon strains, and using comprehensive measurements of athletic and hypoxia performance in individual fish. We believe this paper will be of specific interest to aquaculture professionals who are seeking the enhanced husbandry approaches for achieving higher survival rate over seawater transfer as well as general physiologists. To our knowledge our study is the first to comprehensively illustrate athleticism of domesticated Atlantic salmon from biochemical and cardiorespiratory system levels. Furthermore, we believe this is the first study to show the promising results of enhancing cardiorespiratory system of domesticated Atlantic salmon strain in a hatchery setting. We used a suite of respiratory indices to evaluate athletic robustness and hypoxia performance in individual fish. We discovered that a domesticated strain of Atlantic salmon demonstrated a reduced athleticism and less plasticity in response to a short exercise-training regime compared with a wild strain of Atlantic salmon. We conclude that commercial aquaculture practices may trade off the robustness of the cardiorespiratory system, but not to an extent of completely losing the potential of benefiting from exercise training.
format Article in Journal/Newspaper
author Zhang, Yangfan
Timmerhaus, Gerrit
Anttila, Katja
Mauduit, Florian
Jorgensen, Sven Martin
Kristensen, Torstein
Claireaux, Guy
Takle, Harald
Farrell, Anthony P.
author_facet Zhang, Yangfan
Timmerhaus, Gerrit
Anttila, Katja
Mauduit, Florian
Jorgensen, Sven Martin
Kristensen, Torstein
Claireaux, Guy
Takle, Harald
Farrell, Anthony P.
author_sort Zhang, Yangfan
title Domestication compromises athleticism and respiratory plasticity in response to aerobic exercise training in Atlantic salmon (Salmo salar)
title_short Domestication compromises athleticism and respiratory plasticity in response to aerobic exercise training in Atlantic salmon (Salmo salar)
title_full Domestication compromises athleticism and respiratory plasticity in response to aerobic exercise training in Atlantic salmon (Salmo salar)
title_fullStr Domestication compromises athleticism and respiratory plasticity in response to aerobic exercise training in Atlantic salmon (Salmo salar)
title_full_unstemmed Domestication compromises athleticism and respiratory plasticity in response to aerobic exercise training in Atlantic salmon (Salmo salar)
title_sort domestication compromises athleticism and respiratory plasticity in response to aerobic exercise training in atlantic salmon (salmo salar)
publisher Elsevier Science Bv
publishDate 2016
url https://archimer.ifremer.fr/doc/00334/44518/44214.pdf
https://doi.org/10.1016/j.aquaculture.2016.05.015
https://archimer.ifremer.fr/doc/00334/44518/
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source Aquaculture (0044-8486) (Elsevier Science Bv), 2016-10 , Vol. 463 , P. 79-88
op_relation https://archimer.ifremer.fr/doc/00334/44518/44214.pdf
doi:10.1016/j.aquaculture.2016.05.015
https://archimer.ifremer.fr/doc/00334/44518/
op_rights 2016 Published by Elsevier B.V. All rights reserved.
info:eu-repo/semantics/openAccess
restricted use
op_doi https://doi.org/10.1016/j.aquaculture.2016.05.015
container_title Aquaculture
container_volume 463
container_start_page 79
op_container_end_page 88
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spelling ftarchimer:oai:archimer.ifremer.fr:44518 2023-05-15T15:30:01+02:00 Domestication compromises athleticism and respiratory plasticity in response to aerobic exercise training in Atlantic salmon (Salmo salar) Zhang, Yangfan Timmerhaus, Gerrit Anttila, Katja Mauduit, Florian Jorgensen, Sven Martin Kristensen, Torstein Claireaux, Guy Takle, Harald Farrell, Anthony P. 2016-10 application/pdf https://archimer.ifremer.fr/doc/00334/44518/44214.pdf https://doi.org/10.1016/j.aquaculture.2016.05.015 https://archimer.ifremer.fr/doc/00334/44518/ eng eng Elsevier Science Bv https://archimer.ifremer.fr/doc/00334/44518/44214.pdf doi:10.1016/j.aquaculture.2016.05.015 https://archimer.ifremer.fr/doc/00334/44518/ 2016 Published by Elsevier B.V. All rights reserved. info:eu-repo/semantics/openAccess restricted use Aquaculture (0044-8486) (Elsevier Science Bv), 2016-10 , Vol. 463 , P. 79-88 Athletic robustness Atlantic salmon Domestication Exercise training Hypoxia tolerance Respiratory performance text Publication info:eu-repo/semantics/article 2016 ftarchimer https://doi.org/10.1016/j.aquaculture.2016.05.015 2021-09-23T20:28:27Z Commercially selective breeding of Atlantic salmon (Salmo salar) primarily for rapid growth may compromise cardiorespiratory robustness and its related phenotypes. Therefore, a suite of respiratory indices was used to evaluate aerobic capacity and hypoxia tolerance to test the hypothesis that exercise training can improve the athletic robustness in both domesticated and wild strains of Atlantic salmon, but with the domesticated strain having a less cardiorespiratory plasticity and a lower athletic robustness than the wild strain. We also tested a second hypothesis that a constant acceleration screening protocol should segregate fish according to athletic robustness based on their swimming ability. These hypotheses were tested with parr from Bolaks (domesticated) and Lærdal (wild) strains of Atlantic salmon that were reared under identical hatchery conditions. After screening into either inferior (bottom 20%) or superior (top 20%) swimmers, the four groups of fish (two strains and two swimming performance levels) either were given an 18-day exercise-training regime (an incremental water current of 2.0–2.8 fork lengths s− 1), or were maintained at the control water current (0.5 fork lengths s− 1) for 18 days. Subsequently, fish were sampled for metabolic enzyme analysis in red and white swimming muscles (citrate synthase, CS, and lactate dehydrogenase, LDH; n = 15 from each group) and their individual respiratory capacities were comprehensively assessed by measuring the standard metabolic rate (SMR), maximum rate of oxygen uptake (ṀO2max), absolute aerobic scope (AAS), factorial aerobic scope (FAS), excess post-exercise oxygen consumption (EPOC), critical oxygen level (O2crit) and incipient lethal oxygen saturation (ILOS). Contrary to our expectations, the inferior and superior swimmers were indistinguishable in either strain and these data were pooled. While exercise training produced several tangible benefits for the wild fish, it produced very few for the domesticated fish. For example, the wild strain, but not the domesticated strain, had a significantly higher ṀO2max, AAS and EPOC as a result of training. Also, CS activity in red muscle increased after training to a larger extent in the wild strain than in the domesticated strain. When compared with the wild strain, the domesticated strain had a significantly lower ṀO2max, AAS, FAS and CS activity in white muscle. Thus, the domesticated strain appeared to be athletically less robust than the wild strain. These results imply that approximately ten generations of selective breeding for rapid growth in commercial aquaculture have reduced the overall athletic robustness of domesticated salmon as compared to their wild conspecifics, and given the success in improving athletic robustness of the wild strain, it still remains to be seen whether an exercise training protocol can be developed that will provide benefits to the salmon aquaculture industry. Statement of relevance This manuscript fits perfectly with the scope of aquaculture. We address the possibility that the Norwegian Atlantic salmon (Salmo salar) breeding program that extensively focuses on commercial benefits traits may be compromising the cardiorespiratory system, which may contribute to the mortality of smolts after seawater transfer. We hypothesized that a combination of exercise-screening and exercise-training protocols could select for superior cardiorespiratory performance. This hypothesis was tested by comparing domesticated and wild Norwegian Atlantic salmon strains, and using comprehensive measurements of athletic and hypoxia performance in individual fish. We believe this paper will be of specific interest to aquaculture professionals who are seeking the enhanced husbandry approaches for achieving higher survival rate over seawater transfer as well as general physiologists. To our knowledge our study is the first to comprehensively illustrate athleticism of domesticated Atlantic salmon from biochemical and cardiorespiratory system levels. Furthermore, we believe this is the first study to show the promising results of enhancing cardiorespiratory system of domesticated Atlantic salmon strain in a hatchery setting. We used a suite of respiratory indices to evaluate athletic robustness and hypoxia performance in individual fish. We discovered that a domesticated strain of Atlantic salmon demonstrated a reduced athleticism and less plasticity in response to a short exercise-training regime compared with a wild strain of Atlantic salmon. We conclude that commercial aquaculture practices may trade off the robustness of the cardiorespiratory system, but not to an extent of completely losing the potential of benefiting from exercise training. Article in Journal/Newspaper Atlantic salmon Salmo salar Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer) Aquaculture 463 79 88