Determinants of mercury contamination in viperine snakes, Natrix maura, in Western Europe
Graphical abstract
Introduction
Mercury (Hg) is a well-known environmental contaminant which can originate from both natural and anthropogenic sources (Fitzgerald et al., 2007; Selin, 2009). Atmospheric and water circulation patterns tend to concentrate Hg in aquatic environments (Mason et al., 2012). In addition, anoxic conditions found in slow-moving water bodies promote the transformation of inorganic Hg in methyl-Hg by micro-organisms (Compeau and Bartha, 1985; Jensen and Jernelöv, 1969), which is known for its toxic effects on humans and wildlife (e.g. Tan et al., 2009; Scheuhammer et al., 2008). Finally, Hg can be bioaccumulated within organisms and biomagnified through the food chain, and concentrated in apex predators as fishes, birds or mammals (Mason et al., 1995; Atwell et al., 1998; Power et al., 2002).
Over the last decades, the potential deleterious effects of Hg have been investigated from both an ecological and public health perspective (Driscoll et al., 2013; Lavoie et al., 2013; Eley, 1997; Wolfe et al., 1998). Effects of Hg are multiple and cover a large spectrum of syndromes such as neurological dysfunction (Steuerwald et al., 2000; Basu et al., 2005; Clarkson and Magos, 2006; Scheuhammer and Sandheinrich, 2007; Depew et al., 2012), endocrine disorders (Wada et al., 2009; Meyer et al., 2014) or altered reproduction and offspring quality (Klaper et al., 2006; Burgess and Meyer, 2008; Bergeron et al., 2011; Hopkins et al., 2013a; Tartu et al., 2013). Heretofore, the comprehensive assessments of Hg contamination across complex environments and trophic webs are challenging. Indeed, although the toxic effects of Hg are presumably widespread across the components of aquatic ecosystems, investigations of Hg contamination have been mainly focused on freshwater fish (e.g., Depew et al., 2013; Åkerblom et al., 2014; Scheuhammer et al., 2014; Eagles-Smith et al., 2016), probably because this biota represents both a major source of protein for many human populations (Futsaeter and Wilson, 2013; Dong et al., 2015; Lepak et al., 2016; Fliedner et al., 2016). Aquatic birds have also attracted considerable scientific attention in this respect (Ackerman et al., 2016; Jackson et al., 2016; Blukacz-Richards et al., 2017; Sullivan and Kopec, 2018; Żarski et al., 2017; see also Whitney and Cristol, 2017 for a review). Yet, other aquatic vertebrates than fishes, and especially meso- and apex-predators, may well suffer from Hg contamination (e.g. Driscoll et al., 2007). Such overlooked organisms include amphibians (e.g., Bergeron et al., 2010; Todd et al., 2011), aquatic snakes (e.g., Burger et al., 2005; Drewett et al., 2013), and turtles (e.g., Meyer et al., 2014; Slimani et al., 2017). This is especially true in Western Europe where investigations of Hg contamination in aquatic tetrapods are very scarce as compared with other geographic areas such as Northern America. Nevertheless, inclusion of these organisms is of crucial importance if we are to globally assess Hg contamination worldwide, and in turn to monitor its effects on biodiversity and human health (Gustin et al., 2016).
In addition, some lineages of these overlooked meso- and apex predators also provide a unique set of features that make them useful biological tools to monitor Hg contamination in the wild (e.g., Burger et al., 2005; Slimani et al., 2017). For instance, as compared with highly mobile fish and birds, aquatic reptiles and amphibians are characterized by high levels of philopatry associated with relatively low capacities for large scale movements (Hillman et al., 2014). As a consequence, Hg concentrations in their tissues should strongly reveal those of their relatively small home ranges while highly mobile organisms such as fish and birds may provide information that integrates Hg contamination over large distances, and thus, different environments (Burger et al., 2007; Drewett et al., 2013; Slimani et al., 2017). Additionally, aquatic reptiles are situated relatively high in the trophic web, and as ectotherms, they display relatively low metabolic rates and relatively high tissue conversion rates of their food resources which should enhance their capacity to integrate long-term Hg contamination in their tissues. Characterized by an indeterminate growth, many aquatic reptile species display very wide size range between minute neonates and large adult individuals which allow access to bioaccumulation processes within a population. Finally, easily accessible tissues such as claws in turtles or scales in snakes, in which Hg tends to accumulate and bind to keratins (Hopkins et al., 2013b), provide a powerful opportunity to adopt a non-invasive technique in order to assess Hg contamination in these organisms (Schneider et al., 2015).
In this study, Hg concentrations were investigated in a widely distributed European semi-aquatic Natricinae, the viperine snake (Natrix maura). More than 130 individuals distributed across 6 populations situated in France and Spain were sampled. These populations were associated with contrasted ecological contexts and dominant trophic resources (mainly amphibians in 3 sites and fishes in 3 other sites, Table 1). A non-invasive technique (scale-clipping) was used in order to assay Hg concentrations across this wide geographic area. In addition, on a sub-sample of individuals, scale clipping was combined blood sampling to assess the relationship between Hg concentrations in the blood (reflecting short term Hg exposure, i.e., weeks) and in the scales (integrating Hg exposure over a longer time scale, i.e., months) in this species (as shown in other semi-aquatic snake species, Burger et al., 2005). Specifically, the aims of this study were:
- 1)
to assess Hg contamination in this species across a large ecological context,
- 2)
to investigate bioaccumulation rates across a wide range of body size,
- 3)
and to examine the influence of sex and diet on Hg contamination and bioaccumulation rates.
Section snippets
Study species and study sites
The viperine snake (Natrix maura) is a semi-aquatic freshwater natricine widely distributed across Western Europe and Northern Africa, broadly from France to Morocco (Miras et al., 2015). This relatively small-sized species (up to ~80 cm total length) typically forages for fish and amphibians in aquatic environments such as streams, rivers, marshes, and lakes (Miras et al., 2015; Santos and Llorente, 2009). A skin-shedding occurs in N. maura at the onset of the activity period in early spring,
Scale versus blood Hg concentrations
Hg concentrations between blood and scale clips were positively correlated (F1,6 = 8.87, r2 = 0.59, p = 0.02). However, blood Hg concentrations were 3 times higher than scale Hg concentrations (paired t-test, t = 8.01, p < 0.0001, 0.719 ± 0.267 μg·g−1 versus 0.237 ± 0.195 μg·g−1, respectively).
Determinants of Hg levels
Overall, a significant positive relationship was observed between snake size (SVL) and Hg concentration (F1,130 = 43.95, r2 = 0.25, p < 0.0001). Within sites, the same trend was detectable (all p < 0.005, Fig. 2), except for
Discussion
This study provides an insight into Hg bioaccumulation in a freshwater mesopredator, the viperine snake (N. maura), over a large spatial range and across contrasting habitats. Overall, N. maura do accumulate Hg in their scales. Hg concentrations between blood (short-term Hg exposure, i.e., weeks) and scales (integrating Hg exposure over a longer time scale, i.e., months) were correlated, but that blood display higher Hg concentrations than scale clips. Sex did not seem to influence Hg
Acknowledgements
We thank all the people that were involved in snake surveys, and especially to Mélanie Bouyssou, Pierre Rousseau, Coralie Bossu, Mathieu Normand, Romain Lengagne, Fabrice Conort and Gustavo Cochon. We also thank the staff from the Natural Reserves in which some of our sampling occurred (Réserve Naturelle Nationale de Chérine and de Moëze-Oléron and Réserve Naturelle Régionale de la Tour du Valat in France and the Parque Nacional das Illas Atlanticas de Galicia in Spain), the staff from the
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