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

Biology (Basel). 2023 Apr 10;12(4):577. doi: 10.3390/biology12040577.

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.

Keywords: climate change; elasmobranch; embryogenesis; oxygen loss; predation; sharks.

Grants and funding

The authors would like to thank the Prince Albert II of Monaco Foundation, Intergovernmental Panel on Climate Change (IPCC), and Camões—Instituto da Cooperação e da Língua, I.P. This research is part of project NGANDU funded by the Portuguese Foundation for Science and Technology (FCT) and the Aga Khan Development Network (AKDN) under grant agreement FCT AGA-KHAN/541746579/2019. This work was co-funded by Programa Operacional Regional de Lisboa, Portugal 2020 and the European Union within the project LISBOA-01-0145-FEDER-028609, and by national funds through FCT—Fundação para a Ciência e a Tecnologia within the project Ascend (PTDC/BIA-BMA/28609/2017). All authors acknowledge funding from FCT under the strategic project UIDB/04292/2020 granted to MARE, project LA/P/0069/2020 granted to the Associate Laboratory ARNET, projects UIDP/04378/2020 and UIDB/04378/2020 of the Research Unit on Applied Molecular Biosciences—UCIBIO, and project LA/P/0140/2020 of the Associate Laboratory Institute for Health and Bioeconomy—i4HB. FCT further support this work through PhD grants to SM (SFRH/BD/145276/2019) and CS (SFRH/BD/117890/2016). Further, CS acknowledges the support from the project AGA-KHAN/541746579/2019, financed by FCT and the Aga Khan Development Network (AKDN), through Nova School of Business and Economics. FCT supported JRP through scientific employment stimulus program (2021.01030.CEECIND). TR was funded through an FCT researcher contract (DL57/2016/CP1479/CT0023).