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

Type Article
Date 2016-10
Language English
Author(s) Zhang Yangfan1, 2, Timmerhaus Gerrit3, Anttila Katja4, Mauduit Florian5, 6, Jorgensen Sven Martin3, Kristensen Torstein7, Claireaux Guy5, 6, Takle Harald3, 8, Farrell Anthony P.1, 2
Affiliation(s) 1 : Univ British Columbia, Dept Zool, Vancouver, BC, Canada.
2 : Univ British Columbia, Fac Land & Food Syst, Vancouver, BC, Canada.
3 : Nofima AS, As, Norway.
4 : Univ Turku, Dept Biol, Turku 20014, Finland.
5 : Univ Bretagne Occidentale, Lab Sci Environm Marin LEMAR, Brest, France.
6 : IFREMER, Unite Physiol Fonct Organismes Marins, Plouzane, France.
7 : Nord Univ, Fac Biosci & Aquaculture, Bodo, Norway.
8 : Marine Harvest ASA, Bergen, Norway.
Source Aquaculture (0044-8486) (Elsevier Science Bv), 2016-10 , Vol. 463 , P. 79-88
DOI 10.1016/j.aquaculture.2016.05.015
WOS© Times Cited 43
Keyword(s) Athletic robustness, Atlantic salmon, Domestication, Exercise training, Hypoxia tolerance, Respiratory performance
Abstract 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.
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How to cite 

Zhang Yangfan, Timmerhaus Gerrit, Anttila Katja, Mauduit Florian, Jorgensen Sven Martin, Kristensen Torstein, Claireaux Guy, Takle Harald, Farrell Anthony P. (2016). Domestication compromises athleticism and respiratory plasticity in response to aerobic exercise training in Atlantic salmon (Salmo salar). Aquaculture, 463, 79-88. Publisher's official version : https://doi.org/10.1016/j.aquaculture.2016.05.015 , Open Access version : https://archimer.ifremer.fr/doc/00334/44518/