Seasonal, ontogenetic and sexual changes in lipid metabolism of the small-spotted catshark (Scyliorhinus canicula) in deep-sea free-living conditions

doi:10.1016/j.jembe.2016.07.001

Journal of Experimental Marine Biology and Ecology

Volume 483, October 2016, Pages 59-63

https://doi.org/10.1016/j.jembe.2016.07.001 Get rights and content

Highlights

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Elasmobranchs exhibit variations in nutritional conditions throughout the year.
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Small-spotted catsharks were blood-sampled and released alive.
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Triglycerides and phospholipids differ ontogenetically in the small-spotted catshark.
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Cholesterol levels change seasonally in the small-spotted catshark.
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Lipid metabolites are more influenced by reproduction than nutrition.

Abstract

Marine predators, such as elasmobranchs, exhibit variations in nutritional conditions related to both reproductive traits and food availability in the marine environment throughout the year. The main objective of this study was to examine changes in several blood physiological parameters in a demersal shark, the small-spotted catshark (Scyliorhinus canicula), in the wild in relation to season, sex and maturity stage. For this purpose, 108 individuals at different developmental stages were captured and released alive in the western Mediterranean. Blood was obtained from caudal vessels and plasma lipid fractions (total cholesterol, triglycerides and phospholipids) and a ketone body (3-β-hydroxybutyrate) were measured. During summer, plasma triglyceride and phospholipid levels were lower in adults than in juveniles (mainly in females, probably related to breeding season and laying eggs). Plasma cholesterol levels also showed higher values in summer, indicating higher physical activities during summer and revealing that lipid fractions are more related to reproduction than to nutrition. Plasma 3-β-hydroxybutyrate variations showed a different pattern. No differences were found between sex or maturity stage during summer, although the highest values in adult and juvenile males during winter indicates higher physical activity of males. This study, uses an innovative methodology to establish a correlation between lipid fractions and ketone bodies from the blood of wild individuals and changes in sexual and nutritional status. This method was conducted without damage to the target species and provides new information on the physiology of this abundant elasmobranch in the Mediterranean Sea.

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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To determine the pharmacokinetics of meloxicam in the nursehound shark (Scyliorhinus stellaris) during multiple dose administration.
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A total of eight clinically healthy adult nursehounds (four males, four females).
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No animal died or showed clinical signs of toxicity during the study. Meloxicam administered orally did not produce detectable concentrations in plasma. After intramuscular administration, steady state was achieved after five doses, and mean trough and peak plasma concentrations at steady state were 1.76 ± 0.21 μg mL^–1 and 3.02 ± 0.23 μg mL^–1, respectively. Mean peak concentration accumulation ratio was 2.50 ± 0.22.
This study shows that intramuscular posology produces plasma concentrations considered therapeutic for other species. However, meloxicam was not detected in plasma after oral administration. These results suggest that meloxicam administered intramuscularly may be a useful non-steroid anti-inflammatory drug in nursehound sharks. Further pharmacodynamic studies are needed to fully evaluate its clinical use in this species.
Ecotoxicology applied to conservation: Potential negative metal and metalloid contamination effects on the homeostatic balance of the critically endangered Brazilian guitarfish, Pseudobatos horkelii (Elasmobranchii: Rhinobatidae)
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Metal contamination poses a significant threat to elasmobranchs, underscoring the need for targeted conservation approaches. The critically endangered Brazilian guitarfish, Pseudobatos horkelii, confronts an array of challenges, notably overexploitation, putting its survival at risk. Our study investigated the potential toxicity arising from arsenic (As), cadmium (Cd), mercury (Hg), and lead (Pb) contamination across various adult guitarfish tissues from southeastern Brazil. Serological stress indicators, nutritional metabolites, and creatinine, an organ function marker, were also assessed, and Selenium (Se) levels were also investigated for possible protective effects. Our investigation unveiled significant correlations between metal concentrations and the determined physiological markers, shedding light on potential adverse effects. Remarkably, six correlations were indicative of how Hg and Pb negatively impact hepatic metabolite assimilation, while As was shown to influence renal phosphorus dynamics, Cd to affect rectal gland phosphorus regulation, and Pb to influence creatinine production in muscle tissue. Furthermore, Se demonstrated protective properties against Cd, Hg, and Pb, suggesting a role in alleviating the toxicity of these elements. Despite probable protective Se influences, the detected elemental interactions still suggest potential for organ impairment. These findings gain heightened significance within the context of the cumulative stressors faced by the Brazilian guitarfish, with metal contamination exhibiting the capacity to erode this species resilience against both anthropogenic and environmental pressures, thereby disrupting systemic equilibrium and jeopardizing wild populations. By investigating the intricate balance between metal accumulation and physiological consequences, our study contributes with crucial insights into potential conservation strategy formulations towards pollution for this critically endangered elasmobranch species.
The presence of kelp Lessonia trabeculata drives isotopic niche segregation of redspotted catshark Schroederichthys chilensis
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Citation Excerpt :
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Kelp forests are associated with high biodiversity as they provide habitat and food source for many species. Redspotted catshark Schroederichthys chilensis is a coastal shark species associated with kelp forests of southern South America dominated by Lessonia trabeculata. Despite its common occurrence redspotted catshark the knowledge on its trophic ecology is rudimentary. This study aimed to assess the effects of presence/absence of kelp L. trabeculata on the isotopic niche of redspotted catshark through comparison of δ¹³C and δ¹⁵N in its blood and fin tissues (non-lethal samples). We found that males were characterized by higher trophic position and enriched carbon sources compared to females in locations where kelp was present. In contrast, males and females were characterized by similar isotopic niche in absence of kelp. These differences are most probably an effect of higher prey diversity associated with microhabitats generated by kelp forests that allow sexual segregation of isotopic niche. Therefore, extensive kelp harvest may cause significant effects in isotopic niche and nutritional status of adult redspotted catshark and may negatively affect its populations.
Trophic habits of an abundant shark in the northwestern Mediterranean Sea using an isotopic non-lethal approach
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During July of 2013, a total of 62 small-spotted catshark (Scyliorhinus canicula) individuals were caught in the study area during an experimental demersal fishing cruise (held under the ECOTRANS project; Institute of Marine Sciences ICM-CSIC, Spain). Once caught, the individuals were kept in tanks with a continuous flow of seawater and were sampled within 1 h after capture (Valls et al., 2016). The body length (±0.1 cm), body mass (±0.1 g) and sex (visually examining external reproductive organs) were recorded for each individual.
Studying the feeding ecology of an organism is essential to understanding its ecological role in the ecosystem. Although the small-spotted catshark (Scyliorhinus canicula) is widely studied, most feeding studies have been conducted using invasive techniques, such as the analysis of stomach contents. Moreover, information from the Mediterranean Sea is surprisingly scarce and not up to date. Here, we studied the feeding ecology of the small-spotted catshark in the northwestern Mediterranean Sea using stable isotopes (nitrogen and carbon isotopic values) from blood samples, with individuals released alive in the area of capture after sampling. In overall for the population of small-spotted catshark, the isotopic values were −19.01 ± 1.12‰ and 8.03 ± 0.61‰ for δ¹³C and for δ¹⁵N, respectively. Results reveal a diet mainly composed of euphausiids, with sex and size variations. Results confirm the ecological role of the small-spotted catshark as a mesopredator, which holds a trophic position similar to skates and rays in the study area, but lower than the other demersal and pelagic sharks analysed. The trophic behaviour of the small-spotted catshark indicates its high trophic plasticity, which could allow this species to thrive in highly exploited environments. Our methodological approach, which did not damage the target species, presents new possibilities for conducting ecological studies with other elasmobranchs in the Mediterranean Sea, a highly exploited area that hosts many threatened and rare species.
Carboxylesterase activities in chondrichthyans of the western Mediterranean Sea
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Sharks, rays, skates and chimaeras play an important role as predators in the ecosystems. These species could serve as potential sentinels for the presence of xenobiotics in marine ecosystems. In this study, liver carboxylesterase (CbE) activity was determined for 20 species of chondrichthyans. Carboxylesterase activity, a known esterase involved in the metabolism of pesticides, lipids and certain drugs, was measured using two substrates: 4-nitrophenyl acetate (pNPA) and α-naphthyl acetate (αNA). Rajiformes (rays and skates) showed higher CbE activity than sharks, and the order Chimaeriformes showed the lowest values. In vitro sensitivity to CbE inhibitors was assessed in the shark Scyliorhinus canicula. The substrate αNA was found to be the most adequate as it displayed the highest activity and was more sensitive to the organophosphate dichlorvos in the liver (IC50 = 2.37 μM) and plasma (IC50 = 0.051 μM). The high interspecific variation of CbE activity and its sensitivity to inhibition by fenofibrate suggest that this enzyme could contribute to species-specific differences in drug detoxification.

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Seasonal, ontogenetic and sexual changes in lipid metabolism of the small-spotted catshark (Scyliorhinus canicula) in deep-sea free-living conditions

Highlights

Abstract

Introduction

Section snippets

Sampling procedures

Results

Discussion

Conclusions

Acknowledgments

Comp. Biochem. Physiol. B

Comp. Biochem. Physiol. A Physiol.

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Comp. Biochem. Physiol. A Mol. Integr. Physiol.

Adv. Mar. Biol.

The physiology of fishes

Cascading top-down effects of changing oceanic predator abundances

J. Anim. Ecol.

Production, maturity, reproductive cycle and fecundity of small-spotted catshark, Scyliorhinus canicula (Chondrichthyes: Scyliorhinidae) from the northern coast of Tunisia (Central Mediterranean)

J. Ichthyol.