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

Author:

Varela Jaquelino12ORCID,Martins Sandra13,Court Melanie1ORCID,Santos Catarina Pereira124,Paula José Ricardo15ORCID,Ferreira Inês João678ORCID,Diniz Mário67ORCID,Repolho Tiago15ORCID,Rosa Rui125ORCID

Affiliation:

1. MARE—Marine and Environmetal Sciences Centre/ARNET—Aquatic Research Network, Laboratório Marítimo da Guia, Faculdade de Ciências, Universidade de Lisboa, 2750-374 Cascais, Portugal

2. Sphyrna Association, Sal Rei 5110, Boa Vista Island, Cape Verde

3. Comparative Molecular and Integrative Biology, Centro de Ciências do Mar, Universidade do Algarve, 8005-139 Faro, Portugal

4. Environmental Economics Knowledge Center, Nova School of Business and Economics, New University of Lisbon, 2775-405 Carcavelos, Portugal

5. Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, 2750-374 Cascais, Portugal

6. UCIBIO—Applied Molecular Biosciences Unit, Department of Chemistry, School of Science and Technology, NOVA University Lisbon, 2819-516 Caparica, Portugal

7. Associate Laboratory i4HB, Institute for Health and Bioeconomy, School of Science and Technology, NOVA University Lisbon, 2819-516 Caparica, Portugal

8. LAQV—Associated Laboratory for Green Chemistry—REQUIMTE, Department of Chemistry, School of Science and Technology, NOVA University Lisbon, 2829-516 Caparica, Portugal

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.

Funder

Prince Albert II of Monaco Foundation

NGANDU funded

Programa Operacional Regional de Lisboa, Portugal 2020

national funds

FCT

MARE

Associate Laboratory ARNET

Research Unit on Applied Molecular Biosciences—UCIBIO

Associate Laboratory Institute for Health and Bioeconomy—i4HB

Publisher

MDPI AG

Subject

General Agricultural and Biological Sciences,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology

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