Are fish in hot water? Effects of warming on oxidative stress metabolism in the commercial species Sparus aurata
Graphical abstract
Introduction
One of the main concerns of contemporary society is climate change. Climate projections predict significant changes in ocean chemistry and increases in air and ocean temperature by 2100 (IPCC, 2001, IPCC, 2007, IPCC, 2014, Santos et al., 2002). This has led to a great interest in thermal eco-physiology because temperature is an extremely important factor in aquatic environments, especially considering that most of the inhabiting organisms are ectothermic and cannot regulate their body temperatures. Temperature starts to exert its influence at the kinetic level, impelling biochemical reactions and metabolic rates (Kordas et al., 2011). Its effect builds up to the upper levels of biological organization (i.e. community and ecosystem functioning) by affecting the energy available for growth, foraging and reproduction, which ultimately sets ecological patterns which are related to distribution, abundance of species and biological interactions (Hutchins, 1947, Hochachka and Somero, 2002, Kordas et al., 2011).
In fact, changes in communities and ecosystems have already been detected and attributed to climate change (Walther et al., 2002, Perry et al., 2005, Peck et al., 2012). According to IPCC (2001), southern Europe is one of the regions where warming is expected to be most severe, with predicted air temperature increases up to 4–7 °C by 2100 in the Iberian Peninsula (Santos et al., 2002 – SIAM Project). More specifically, climate change models predict a +2–3 °C increase in Portuguese waters (Miranda et al., 2002) and +3–4 °C in the Mediterranean (Fischer and Schär, 2010). In this context, species inhabiting these areas, which are already warm, will be exposed to even higher temperatures, especially considering that heat waves will also increase in frequency, duration and intensity (IPCC, 2007). Therefore, it is relevant to understand the physiological and molecular responses deployed by fish to cope with ocean warming.
Several parameters and end-points have been used in the field of eco-physiology to detect changes on the health of wild and cultured fish. According to Blier (2014) oxidative stress is an emerging concept used to assess the metabolic status and health of organisms, which in turn are valuable tools in management and conservation of wild populations. These authors also state that such assessments are useful for the management and conservation of wild populations. Oxidative stress results from the excessive production of reactive oxygen species (ROS), in a way that the buffering effect of antioxidant agents is not enough to prevent the damaging effects of ROS, leading to a disturbance in cell homeostasis and possible cell death (Halliwell and Gutteridge, 1999, Ahmed, 2005, Heise et al., 2006, Blier, 2014). In marine organisms, high temperature increases ROS production due to higher respiratory rates and hypoxia followed by re-oxygenation of tissues after temporary stressful events (Halliwell and Gutteridge, 1999, Abele et al., 2002, Freire et al., 2011). Several studies in marine organisms have shown that oxidative stress products change in response to temperature and in order to cope with such stress, animals produce antioxidant enzymes that neutralize ROS e.g. catalase, superoxide dismutase and glutathione-S-transferase and peroxidase (Padmini et al., 2009, Madeira et al., 2013, Madeira et al., 2014a, Vinagre et al., 2014a, Vinagre et al., 2014b). However, when these defenses are not strong enough and stress is severe, organisms can experience the deleterious effects of oxidative damage such as DNA degradation, lipid peroxidation and protein carbonylation (see Abele and Puntarulo, 2004, Lesser, 2006), which can be exacerbated under climate change scenarios and heat wave events. Such warming events and associated oxidative stress may have serious impacts on organismal health, potentially affecting biological processes such as spawning, mortality rates and recruitment success (e.g. Randall and Szmant, 2009, Ross et al., 2013, Jeffries et al., 2014, Hemmer-Brepson et al., 2014). This is especially relevant in organisms inhabiting shallow waters (i.e. little thermal inertia) like juvenile fish that inhabit nursery grounds such as estuaries and coastal lagoons. Thus, the model species chosen for this study was the sea bream Sparus aurata (Linnaeus 1758). This is a commercial species, highly captured and cultured in Europe (see FAO, FishStat Sparus aurata, 2015). It has a subtropical distribution, occurring in Eastern Atlantic (British Isles to Cape Verde), and the Mediterranean and Black Seas (Froese and Pauly, 2006, Sola et al., 2007). This species lives in sandy bottoms and seagrass beds, with a demersal juvenile phase occurring in shallow waters (down to 30 m deep). Larvae/juveniles migrate to nursery grounds, passing through several thermal regimes, with varying temperatures (mean of 15–16 °C in coastal waters to 24–26 °C in nursery grounds), which can be stressful to young fish. Considering this background, the aims of the present work were to assess the health status and vulnerability/resistance of S. aurata juveniles to ocean warming and heat wave events by (1) exposing fish to a thermal ramp until Critical Thermal Maximum is reached and (2) quantifying oxidative stress biomarkers in several organs, including oxidative damage products i.e. lipid peroxidation (LPO), and antioxidant enzymes i.e. catalase, superoxide dismutase, glutathione-S-transferase, and cytochrome CYP1A. This is especially relevant considering that thermal-induced oxidative damage can affect capture production, as well as mortality and meat quality in fish farms.
Section snippets
Ethical statements
This study was carried out in strict accordance with the recommendations of the Portuguese legislation for animal experimentation following the approval of Direcção Geral de Alimentação e Veterinária. Moreover, the three authors have a level C certification by FELASA (Federation of European Laboratory Animal Science Associations). All efforts were made to minimize animal suffering.
Thermal ramp trial
Juvenile fish of S. aurata (mean ± SD total length of 92.1 ± 8.1 mm and 12.2 ± 2.9 g in weight) were obtained from a fish
Results
To simplify figure interpretation, all statistical differences highlighted correspond only to significant differences found in the temperature treatments when compared to the control group (18 °C).
Discussion
In the present study, juveniles of S. aurata showed an increased oxidative stress response in several tissues, especially muscle and liver. This is in accordance with other studies that state that increased temperature levels lead to oxidative stress in ectothermic organisms (e.g. Bagnyukova et al., 2007, Madeira et al., 2013, Vinagre et al., 2014b). As expected, antioxidant enzymes generally increased their activities to counterbalance the effects of oxidative damage, being an important
Conclusions
Several authors have reported that climate change effects are disturbing marine biological processes from genes to ecosystems, impacting goods and services provided to society (e.g. Brierley and Kingsford, 2009). Therefore, scientists have to face the challenge of improving the predictive power of ecological forecasting (Kordas et al., 2011). Physiology plays a crucial role in biological up scaling because it integrates mechanisms from the molecular level to the individual level and further on (
Acknowledgements
The authors would like to thank Marta Martins, Ana Patrícia and Carolina Madeira for the help given in the maintenance of experimental systems and feeding of the organisms. Authors would like to thank MARESA for providing Sparus aurata juveniles. The authors have no conflicts of interest to declare. This study had the support of the Portuguese Fundação para a Ciência e a Tecnologia (FCT) [individual grants: senior researcher position to C.V., SFRH/BD/80613/2011 to D.M.; project grants
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