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Impacts of Deoxygenation and Hypoxia on Shark Embryos Anti-Predator Behavior and Oxidative Stress

SIMPLE SUMMARY: Despite their importance, sharks are among the most endangered ocean species. In addition to overexploitation and the destruction of their natural habitat, climate change is also known to pose a serious threat to them. Among the physico-chemical changes associated with climate change...

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Autores principales: Varela, Jaquelino, Martins, Sandra, Court, Melanie, Santos, Catarina Pereira, Paula, José Ricardo, Ferreira, Inês João, Diniz, Mário, Repolho, Tiago, Rosa, Rui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10136306/
https://www.ncbi.nlm.nih.gov/pubmed/37106777
http://dx.doi.org/10.3390/biology12040577
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author Varela, Jaquelino
Martins, Sandra
Court, Melanie
Santos, Catarina Pereira
Paula, José Ricardo
Ferreira, Inês João
Diniz, Mário
Repolho, Tiago
Rosa, Rui
author_facet Varela, Jaquelino
Martins, Sandra
Court, Melanie
Santos, Catarina Pereira
Paula, José Ricardo
Ferreira, Inês João
Diniz, Mário
Repolho, Tiago
Rosa, Rui
author_sort Varela, Jaquelino
collection PubMed
description SIMPLE SUMMARY: Despite their importance, sharks are among the most endangered ocean species. In addition to overexploitation and the destruction of their natural habitat, climate change is also known to pose a serious threat to them. Among the physico-chemical changes associated with climate change, oxygen loss has been the least studied in terms of its effect on shark physiology and behavior. In this study, we evaluated the impact of deoxygenation (93% air saturation) and hypoxia (26% air saturation) on the anti-predatory behavior and physiology of temperate shark embryos. We found that hypoxia caused a high mortality (44%), significantly increased embryo movement within capsules, and, consequently, reduced the freezing response behavior (a behavior that allows embryos to be unnoticed by predators). Regarding oxidative stress, most biomarkers analyzed were not impacted by the experimental treatments. Overall, our results suggest that the temperate shark’s early life stages showed a certain degree of resilience to deoxygenation but not to hypoxia. ABSTRACT: Climate change is leading to the loss of oxygen content in the oceans and endangering the survival of many marine species. Due to sea surface temperature warming and changing circulation, the ocean has become more stratified and is consequently losing its oxygen content. Oviparous elasmobranchs are particularly vulnerable as they lay their eggs in coastal and shallow areas, where they experience significant oscillations in oxygen levels. Here, we investigated the effects of deoxygenation (93% air saturation) and hypoxia (26% air saturation) during a short-term period (six days) on the anti-predator avoidance behavior and physiology (oxidative stress) of small-spotted catshark (Scyliorhinus canicula) embryos. Their survival rate decreased to 88% and 56% under deoxygenation and hypoxia, respectively. The tail beat rates were significantly enhanced in the embryos under hypoxia compared to those exposed to deoxygenation and control conditions, and the freeze response duration showed a significant opposite trend. Yet, at the physiological level, through the analyses of key biomarkers (SOD, CAT, GPx, and GST activities as well as HSP70, Ubiquitin, and MDA levels), we found no evidence of increased oxidative stress and cell damage under hypoxia. Thus, the present findings show that the projected end-of-the-century deoxygenation levels elicit neglectable biological effects on shark embryos. On the other hand, hypoxia causes a high embryo mortality rate. Additionally, hypoxia makes embryos more vulnerable to predators, because the increased tail beat frequency will enhance the release of chemical and physical cues that can be detected by predators. The shortening of the shark freeze response under hypoxia also makes the embryos more prone to predation.
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spelling pubmed-101363062023-04-28 Impacts of Deoxygenation and Hypoxia on Shark Embryos Anti-Predator Behavior and Oxidative Stress Varela, Jaquelino Martins, Sandra Court, Melanie Santos, Catarina Pereira Paula, José Ricardo Ferreira, Inês João Diniz, Mário Repolho, Tiago Rosa, Rui Biology (Basel) Article SIMPLE SUMMARY: Despite their importance, sharks are among the most endangered ocean species. In addition to overexploitation and the destruction of their natural habitat, climate change is also known to pose a serious threat to them. Among the physico-chemical changes associated with climate change, oxygen loss has been the least studied in terms of its effect on shark physiology and behavior. In this study, we evaluated the impact of deoxygenation (93% air saturation) and hypoxia (26% air saturation) on the anti-predatory behavior and physiology of temperate shark embryos. We found that hypoxia caused a high mortality (44%), significantly increased embryo movement within capsules, and, consequently, reduced the freezing response behavior (a behavior that allows embryos to be unnoticed by predators). Regarding oxidative stress, most biomarkers analyzed were not impacted by the experimental treatments. Overall, our results suggest that the temperate shark’s early life stages showed a certain degree of resilience to deoxygenation but not to hypoxia. ABSTRACT: Climate change is leading to the loss of oxygen content in the oceans and endangering the survival of many marine species. Due to sea surface temperature warming and changing circulation, the ocean has become more stratified and is consequently losing its oxygen content. Oviparous elasmobranchs are particularly vulnerable as they lay their eggs in coastal and shallow areas, where they experience significant oscillations in oxygen levels. Here, we investigated the effects of deoxygenation (93% air saturation) and hypoxia (26% air saturation) during a short-term period (six days) on the anti-predator avoidance behavior and physiology (oxidative stress) of small-spotted catshark (Scyliorhinus canicula) embryos. Their survival rate decreased to 88% and 56% under deoxygenation and hypoxia, respectively. The tail beat rates were significantly enhanced in the embryos under hypoxia compared to those exposed to deoxygenation and control conditions, and the freeze response duration showed a significant opposite trend. Yet, at the physiological level, through the analyses of key biomarkers (SOD, CAT, GPx, and GST activities as well as HSP70, Ubiquitin, and MDA levels), we found no evidence of increased oxidative stress and cell damage under hypoxia. Thus, the present findings show that the projected end-of-the-century deoxygenation levels elicit neglectable biological effects on shark embryos. On the other hand, hypoxia causes a high embryo mortality rate. Additionally, hypoxia makes embryos more vulnerable to predators, because the increased tail beat frequency will enhance the release of chemical and physical cues that can be detected by predators. The shortening of the shark freeze response under hypoxia also makes the embryos more prone to predation. MDPI 2023-04-10 /pmc/articles/PMC10136306/ /pubmed/37106777 http://dx.doi.org/10.3390/biology12040577 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Varela, Jaquelino
Martins, Sandra
Court, Melanie
Santos, Catarina Pereira
Paula, José Ricardo
Ferreira, Inês João
Diniz, Mário
Repolho, Tiago
Rosa, Rui
Impacts of Deoxygenation and Hypoxia on Shark Embryos Anti-Predator Behavior and Oxidative Stress
title Impacts of Deoxygenation and Hypoxia on Shark Embryos Anti-Predator Behavior and Oxidative Stress
title_full Impacts of Deoxygenation and Hypoxia on Shark Embryos Anti-Predator Behavior and Oxidative Stress
title_fullStr Impacts of Deoxygenation and Hypoxia on Shark Embryos Anti-Predator Behavior and Oxidative Stress
title_full_unstemmed Impacts of Deoxygenation and Hypoxia on Shark Embryos Anti-Predator Behavior and Oxidative Stress
title_short Impacts of Deoxygenation and Hypoxia on Shark Embryos Anti-Predator Behavior and Oxidative Stress
title_sort impacts of deoxygenation and hypoxia on shark embryos anti-predator behavior and oxidative stress
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10136306/
https://www.ncbi.nlm.nih.gov/pubmed/37106777
http://dx.doi.org/10.3390/biology12040577
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