Seasonal, ontogenetic and sexual changes in lipid metabolism of the small-spotted catshark (Scyliorhinus canicula) in deep-sea free-living conditions
Introduction
Sharks are considered key species in marine ecosystems due to their role in maintaining the structure and functioning of food webs (Baum and Worm 2009). They are highly sensitive to ecosystem changes including human impacts (Myers et al., 2007, Dulvy et al., 2014). In comparison with other predators such as seabirds or marine mammals, few ecophysiological studies have been conducted in free-living elasmobranchs (García-Garrido and Muñoz-Chapuli, 1990, Speers-Roesch and Treberg, 2010, Carrier et al., 2012, Gallagher et al., 2014). Such studies would be a huge step toward understanding how environmental seasonal changes or ontogeny/sexual variations in particular nutritional requirements affect the physiology of these marine predators. For example, variations in the quality or quantity of prey in the environment during the year can affect the physiological status of elasmobranchs (Pethybridge et al. 2014). Similarly, due to differences in the reproductive requirements or the morphology and behaviour between males and females, some variations in particular physiological parameters associated with reproduction may be present (Wearmouth and Sims 2008).
The physiology of elasmobranchs can be studied by measuring particular blood metabolites related to nutritional stores (García-Garrido and Muñoz-Chapuli, 1990, Ballantyne, 2014, Gallagher et al., 2014). Thus, plasma levels of total cholesterol or triglycerides are useful indicators of the use of lipid reserves and of animal condition (García-Garrido et al., 1990). Although elasmobranches usually present low levels of blood cholesterol or triglycerides (Crabtree et al. 1972), increments in these metabolites indicate the mobilisation of lipid stores as a consequence of variations in the energy requirements associated with reproduction or body condition (García-Garrido et al., 1990). Similarly, an increase in ketone bodies in the blood, such as 3-β-hydroxybutyrate, indicates higher muscular activity or the mobilisation of lipid reserves during starvation situations (Ballantyne, 1997, Speers-Roesch, 2006). Plasma levels of the ketone body 3-β-hydroxybutyrate in elasmobranches are as high as those seen in fasted mammals, indicating their preference for ketone body oxidation rather than fatty acid oxidation in muscle under routine conditions (Speers-Roesch and Treberg 2010).
In the present study, the physiological state (plasma biochemistry) of the small-spotted catshark (Scyliorhinus canicula) was examined in free-living conditions. The small-spotted catshark is a widespread and abundant elasmobranch particularly appropriate as an experimental model due its strong resistance to handling and the relative ease of capture. Despite these facilities, there is a surprising scarcity of studies on the ecophysiology in free-living conditions of this shark species. This is an abundant demersal shark present throughout the Mediterranean Sea and in some areas of the Atlantic Ocean (Navarro et al. 2016). Similar to several sharks, the small-spotted catshark is oviparous, laying eggs enveloped in a shielding sleeve and anchored in algae and other solid structures (Ellis and Shackley 1997). Males and females are sexually active throughout the year (Capapé et al. 2014). In relation to food habits, the small-spotted catshark is a nocturnal opportunistic predator that exploits a wide range of benthic crustaceans and demersal fish (Valls et al. 2011). The main aims of the present study were to examine the effect of season (winter and summer), sex (males and females) and maturity stage (juveniles and adults) on three plasma lipid parameters (cholesterol, triglyceride, phospholipids) and one ketone body (3-β-hydroxybutyrate).
Section snippets
Sampling procedures
The study was conducted at the mouth of the Ebro River, in the western Mediterranean Sea (Fig. 1). This is a relatively highly productive area in the Mediterranean Sea due to the combination of the contributions of organic matter by the Ebro River in the wider area of the continental shelf, and the effect of the Liguro-Provençal-Catalan current along the slope of the continental platform (Estrada, 1996, Salat, 1996). During winter (February) and summer (July) of 2013, a total of 108
Results
Total body weight and length, and plasma levels of the plasma indicators of lipid metabolism of small-spotted catshark (Scyliorhinus canicula) are shown in Table 1. All the plasma lipid fractions analysed showed significant differences according to the season (Table 2), being on average higher in the summer. Nevertheless, the state of maturity presented interactions with sex in the case of total cholesterol and with season for triglycerides and phospholipids (Table 2). Cholesterol showed higher
Discussion
Our results show changes in plasma lipid fractions (triglycerides, phospholipids and cholesterol) and the ketone body, indicating that the mobilisation of these reserves from the liver of the small-spotted catshark (the main organ for lipid storage in elasmobranchs) to extra hepatic tissues is related to the season (summer and winter), sex (males and females) and maturity stage (juveniles and adults). All plasma lipid fractions, on average, were higher in summer, probably in relation to food
Conclusions
The present study provides for the first time physiological information on the small-spotted catshark in free-living conditions in the western Mediterranean Sea. The results revealed seasonal and sexual variations in body mass, plasma lipid fractions and 3-β-hydroxybutyrate, indicating that adult females mobilize lipid reserves for the formation of egg-yolk, while adult males show high values of ketone bodies during winter probably associated with an increase in physical activity. The approach
Acknowledgments
A special thanks to Isabel Palomera and the entire crew of the ECOTRANS oceanographic cruises for their help in the present study. This study forms a contribution to the project ECOTRANS (CTM2011-26333, Spanish Ministry of Economy and Competitiveness, Spain) and to the master's thesis of EV. JN was supported by the Andalucía Talent Hub Program launched by the Andalusian Knowledge Agency, co-funded by the European Union's Seventh Framework Program, Marie Skłodowska-Curie actions (COFUND Grant
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