Blue sharks (Prionace glauca) as bioindicators of pollution and health in the Atlantic Ocean: Contamination levels and biochemical stress responses
Graphical abstract
Introduction
Marine ecosystems are being continuously loaded with xenobiotics produced by human activities, very often affecting aquatic organisms (Van der Oost et al., 2003). Persistent organic pollutants (POPs), such as polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), polychlorinated biphenyls (PCBs), brominated flame retardants (BFRs) and perfluorinated compounds (PFCs), or metals such as arsenic (As), cadmium (Cd), copper (Cu), iron (Fe), mercury (Hg), manganese (Mn), nickel (Ni), lead (Pb) and zinc (Zn) can negatively affect marine fauna and human health given their high toxicity and persistence in the environment, leading to bioaccumulation processes (Heath, 1995, Storelli et al., 2002, Gramatica and Papa, 2007, Storelli et al., 2011, Skomal and Mandelman, 2012, Barrera-García et al., 2013). Bioaccumulation of these xenobiotics is a growing concern and has been shown to cause injurious effects on biodiversity (Franke et al., 1994, Marchettini et al., 2001, Wang, 2002).
The changes caused by pollutants in the ecosystem usually have an earlier effect at lower levels of biological organization, such as at the organism level or even at the gene and cellular level, allowing the development of biomarkers to monitor changes caused by the contaminants, before they cause an effect at higher complexity levels – communities or ecosystems (Bayne et al., 1985, Lemos et al., 2010). In order to assess the health of marine ecosystems, different biological parameters with the potential to be used as biomarkers may be of use, such as oxidative stress related enzymatic activities, DNA damage and lipid peroxidation (LPO) as measurements of oxidative damage, and indicators of neuromuscular activity and energy expenditure (Winston and Di Giulio, 1991, Filho, 1996, Van der Oost et al., 2003).
Usually, when a contaminant enters a living organism, a two-phase detoxification process is initiated in order to facilitate its elimination (Chen, 2012). Glutathione-S-transferase (GST) plays a role in the second phase of the detoxification process, where it facilitates the excretion of xenobiotics (Van der Oost et al., 2003). This process is essential but increases the already naturally occurring cellular oxidation (Valko et al., 2007). Furthermore, the presence of POPs and metal contaminants further increases the amount of reactive oxygen species (ROS), such as superoxide anion radical (O2•−) and hydrogen peroxide (H2O2), forcing the cells to fight the harmful effects of these oxidizing molecules (Buet et al., 2006, Kumar et al., 2014). Defence mechanisms to eliminate ROS, and prevent oxidative damage, include enzymatic antioxidants, such as superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx) and glutathione reductase (GR). SOD is an enzyme responsible for the transformation of O2•− into H2O2 that is then eliminated by the enzymes CAT and GPx, both acting to prevent its accumulation. GR ensures that reduced glutathione (GSH) is available to act as an antioxidant itself, or as a cofactor for GPx and GST (Egaas et al., 1995, Halliwell and Gutteridge, 2001, Livingstone, 2001, Richardson et al., 2008, Valko et al., 2007).
All the internal responses of the organisms to cope with pollution stress are highly energy-costly. Examples of biomarkers that can be used to assess effects related with changes in the energy metabolism are the enzymes lactate dehydrogenase (LDH) and isocitrate dehydrogenase (IDH), which are involved in the anaerobic and aerobic metabolism, respectively (Bernal et al., 2003, Walsh et al., 2006), and have been successfully applied in studies addressing effects of marine contamination by metals (e.g. Antognelli et al., 2003, Vieira et al., 2009), or by different organic pollutants (e.g. Monteiro et al., 2006, Greco et al., 2007).
Acetylcholinesterase (AChE), a vital enzyme for good neuronal functions in vertebrates, is highly sensitive to anti-cholinergic compounds and other contaminants often present in marine ecosystems, and has already demonstrated great potential to be used in pollution monitoring studies as a biomarker of effect (Payne et al., 1996, Kirby et al., 2000, Van der Oost et al., 2003, Arufe et al., 2007, Solé et al., 2008, Alves et al., 2015).
Due to their role as apex predators, elasmobranchs such as sharks end up being more exposed to environmental contamination through bioaccumulation and biomagnification processes through the food web (Serrano et al., 2000, Strid et al., 2007). Additionally, their wide distribution and importance to the ecosystem makes them ideal sentinel organisms for marine pollution biomonitoring studies (Marcovecchio et al., 1991, Vas, 1991). Sharks are known to accumulate high concentrations of metals (Storelli et al., 2002, Pethybridge et al., 2010, Storelli and Marcotrigiano, 2004, Turoczy et al., 2000). Some of them are essential for physiological processes (e.g., Fe and Zn), while others do not have any recognized physiological purpose (e.g., Hg and Pb) (Barrera-García et al., 2013). To know the concentrations of these metals present in fish muscle, and particularly Hg, is of utmost importance since in most cases this is the main route of exposure to these elements in humans (Järup, 2003, Khayatzadeh and Abbasi, 2010). Furthermore, Hg can be found in different forms and one of the most toxic, methylmercury (meHg), accounts for > 95% of the total Hg found in the muscle of fishes (Krystek and Ritsema, 2005, Piraino and Taylor, 2009, Payne and Taylor, 2010). Sharks have also been found to accumulate large amounts of POPs in their muscle and liver tissues (e.g., Johnson-Restrepo et al., 2005, Storelli et al., 2005, Storelli et al., 2011). These compounds have even been found in sharks from remote areas as the Artic (Strid et al., 2007), and they can severely impair the health of both marine organisms and humans (Mandal, 2005, Foster et al., 2012).
The blue shark (Prionace glauca, L. 1758) is one of the most frequently caught shark species all over the world and in particular by the Portuguese longline swordfish fishing fleet as bycatch (Bonfil, 1994, Santos et al., 2002, Stevens, 2009). Some recent studies have demonstrated the potential of this species to be used as a biomonitor of marine contamination (Storelli et al., 2011, Barrera-García et al., 2012, Barrera-García et al., 2013), but very little is known about the mechanisms involved in these sharks' detoxification and antioxidant processes, or other mechanisms of response to chemical pollutants. Understanding these relations is of upmost importance to public health since almost 122,000 t of shark meat were imported worldwide in 2011, with P. glauca increasingly becoming the preferential source of both fins and meat (Dent and Clarke, 2015, Eriksson and Clarke, 2015).
The main objective of the present study is two-folded: 1) Do Atlantic blue sharks present high levels of POPs and metals in their tissues that can pose a risk for these organisms as well as for humans health?; and 2) Are the contaminant body burden levels correlated with biochemical responses of stress in the organisms?
With this approach, reliable biomarkers for P. glauca can be addressed as prospect tools for biomonitoring Atlantic waters. Also, to our knowledge, this is one of the most comprehensive studies of its kind, attempting to integrate the levels of different contamination sources (e.g. metals and POPs) with detoxification pathways, oxidative stress response mechanisms, and energetic and neuronal parameters in sharks.
Section snippets
Organisms
Twenty P. glauca individuals were captured at a depth of approximately 20 m, southwest of Portugal (36°43′11.2″N, 13°09′30.0″W), aboard a commercial swordfishing vessel as bycatch. Captured sharks were sacrificed by the fisherman after landing on the vessel, and the procedure of capture and handling was performed as fast as possible and in a similar way between individuals. Immediately after capture, tissues (liver, muscle, and brain) were collected from each individual taking the appropriate
Results
The 20 sharks sampled in the present study consisted of 12 females and 8 males, and ranged from 112 to 167 cm total length (TL). Although all individuals were considered juveniles, samples were also grouped according to sex and size, in order to assess eventual effects of these physiological characteristics. Size groups were defined as: 1) individuals with < 130 cm TL (lower than the average TL); and 2) individuals over 130 cm TL (higher than the average TL).
Discussion
Marine apex predators are known to accumulate higher levels of pollutants in their bodies than the majority of other animals in their food chain (Storelli et al., 2005, Storelli et al., 2007, Storelli et al., 2008, Storelli and Marcotrigiano, 2006). It is therefore of upmost importance to understand if and how these pollutants might affect the organisms, as all changes, even if seemingly inconsequential, might affect their physiology and natural behaviour which can have repercussions in the
Acknowledgements
This study had the support of the Fundação para a Ciência e a Tecnologia (FCT) Strategic Project UID/MAR/04292/2013 granted to MARE. Sara C. Novais wish to acknowledge the financial support given by FCT (SFRH/BPD/94500/2013).
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