Snakes As Novel Biomarkers of Mercury Contamination: a Review

Snakes as Novel Biomarkers of Mercury Contamination: A Review David L. Haskins, Robert M. Gogal Jr., and Tracey D. Tuberville Contents 1 Introduction .................................................................................. 134 1.1 Snakes, Ecotoxicology, and Mercury ................................................. 134 2 Mercury ...................................................................................... 135 2.1 Mercury Sources ....................................................................... 135 2.2 Forms of Mercury and Availability in the Environment ... .......................... 136 3 Snakes as Biomarkers of Mercury Exposure ............................................... 136 4 Mercury Bioaccumulation in Snakes ....................................................... 137 5 Effects of Mercury on Snake Health and Immune Status .................................. 144 5.1 Mercury Effects in Wildlife ........................................................... 144 5.2 Maternally Transferred Mercury in Snakes ........................................... 144 5.3 Mercury and Reptile Immunotoxicology ............................................. 145 6 Snakes and Mercury Transfer ............................................................... 145 6.1 Snakes and Mercury Transfer in Aquatic and Terrestrial Ecosystems ............... 145 6.2 Snakes and Risk of Human Exposure to Contaminants .............................. 146 7 Conclusions .................................................................................. 147 8 Summary ..................................................................................... 147 References ....................................................................................... 148 D. L. Haskins (*) Savannah River Ecology Laboratory, University of Georgia, Aiken, SC, USA Interdisciplinary Toxicology Program, University of Georgia, Athens, GA, USA Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA, USA e-mail: [email protected] R. M. Gogal Jr. Department of Biosciences and Diagnostic Imaging, College of Veterinary Medicine, University of Georgia, Athens, GA, USA e-mail: [email protected] T. D. Tuberville Savannah River Ecology Laboratory, University of Georgia, Aiken, SC, USA e-mail: [email protected] © Springer Nature Switzerland AG 2019 133 P. de Voogt (ed.), Reviews of Environmental Contamination and Toxicology, Volume 249, Reviews of Environmental Contamination and Toxicology Volume 249, https://doi.org/10.1007/398_2019_26 134 D. L. Haskins et al. 1 Introduction 1.1 Snakes, Ecotoxicology, and Mercury Ecological risk assessments are a tool used by regulatory agencies to determine how the environment and associated wildlife might be impacted by proposed or ongoing anthropogenic activities (Newman 2015). In the last two decades, researchers have highlighted the absence of reptiles in these assessments (Campbell and Campbell 2001; Grillitsch and Schiesari 2010; Weir et al. 2010). Reptiles are often underrep- resented or excluded from ecological risk assessments even though they serve important roles in their ecosystems and can be both predators and prey of terrestrial and aquatic species. Furthermore, reptiles often inhabit environments that are conducive to long-term retention of contaminants (e.g., methylation of mercury in isolated wetlands), increasing the likelihood that they will be exposed to and accumulate pollutants. Physiological characteristics found in reptiles also make them ideal study candidates for risk assessments. Their metabolic mode (ectothermy) allows high tissue conversion rates and low tissue turnover rates, which may promote processes associated with bioaccumulation (Hopkins 2006). Many of these organisms also exhibit indeterminate growth, and this may allow researchers to quantify bioaccumulation rates over their entire lifespan. Although interest in reptile ecotoxicology has increased in recent years, snakes are still widely excluded from such studies, even though their life history characteristics make them useful candidate receptor species (Hopkins 2000; Campbell and Campbell 2001; Drewett et al. 2013). This is likely due to a combination of factors. For instance, snake studies have historically been plagued by small sample sizes, and thus, accumulation of information regarding their life history and ecological traits has lagged behind other reptiles. Many species are also secretive, limiting their detection or capture (Durso et al. 2011; Willson and Winne 2016; Willson et al. 2011). Because of these issues, research involving these species may be more difficult to conduct and interpret. Cultural biases toward snakes are also often extreme, and people tend to either worship or loathe these reptiles (Pough et al. 1998; Campbell and Campbell 2001). Further, it is often difficult to convince funding agencies and the general public that results from snake studies positively impact humans, although environmental education efforts may be helping in this regard (Shine and Bonnet 2000). Overall, it is no surprise that research in reptile ecotoxicology has significantly lagged behind that of other taxonomic groups (Hopkins 2000; Weir et al. 2010). There are more than 3,000 species of snakes recognized globally, and they exhibit a wide diversity in their habitat associations. These limbless predators inhabit every continent except Antarctica and have successfully colonized terrestrial, freshwater, and marine habitats (Vitt and Caldwell 2014). Of the snake families, Colubridae is the most speciose and is comprised of more than half of the world’s described snake species (>1,700 species, Vitt and Caldwell 2014). Although the ICUN Red List of Threatened Species does not indicate that large numbers of snake species are Snakes as Novel Biomarkers of Mercury Contamination: A Review 135 threatened (~185 at risk, IUCN 2017), it is notoriously difficult to study snake population dynamics, and recent research has suggested that snakes (like other reptiles) could be experiencing population declines likely due to an assortment of threats, including pollution (Gibbons et al. 2000; Reading et al. 2010). Mercury (Hg) is a major contaminant of concern around the globe, and its prevalence has increased markedly in both terrestrial and aquatic habitats over the last half a century (Tweedy et al. 2013; Lamborg et al. 2014). Anthropogenic activities such as mining, coal combustion, and other industrial processes have facilitated Hg’s release into the environment, where it is transformed into a bioavailable form (methylmercury, MeHg) that can accumulate in wildlife (Schneider et al. 2013). Recent studies suggest that snakes can accumulate significant amounts of Hg, with snakes inhabiting aquatic environments often exhibiting the highest Hg burdens (Axelrad et al. 2011; Drewett et al. 2013). Indeed, most ecotoxicological studies of Hg bioaccumulation in snakes have focused on aquatic or semiaquatic species such as cottonmouths (Agkistrodon piscivorus), natricines (e.g., Nerodia and Thamnophis spp.), and a few other colubrids (Campbell and Campbell 2001; Schneider et al. 2013; Lemaire et al. 2018). In this review, we will examine the sources of Hg contamination and the factors that determine availability within aquatic and terrestrial environments. We will also review the potential of snakes as biomarkers for Hg exposure, focusing on bioaccumulation and known effects of exposure. We will then discuss the role snakes play in nutrient and contaminant transfer. Finally, we will conclude by identifying research gaps. 2 Mercury 2.1 Mercury Sources Mercury is a highly toxic heavy metal that is released into the environment by natural and anthropogenic sources. Unlike other heavy metals of concern (e.g., lead or cadmium), Hg is unique not only because is it locally transformed to more bioavailable forms (e.g., Hg methylation), but because it also can be transported on a global scale via atmospheric cycling and deposition (Boening 2000; Zhang et al. 2009). In fact, distinct atmospheric cycles may result in a system where regions can be impacted by Hg that originates from both local and global inputs. Prior to the industrial revolution, Hg in the environment mostly originated from the natural mobilization of Hg deposits in the earth’s crust and volcanoes (Selin 2009). Pres- ently, environmental Hg originates from a variety of anthropogenic activities, including coal burning, mining, water treatment plants, and other industrial facilities (Selin 2009). Thus, industrialization has significantly altered Hg emissions and cycling. For example, one study recently suggested that Hg concentrations in ocean surface waters have tripled compared to pre-anthropogenic conditions (Lamborg et al. 2014). 136 D. L. Haskins et al. 2.2 Forms of Mercury and Availability in the Environment The major forms of Hg in the environment include elemental, ionic, or organic Hg (e.g., methylmercury or MeHg). Atmospheric Hg is primarily comprised of elemental Hg, which has a long atmospheric lifespan (~1 year) and thus contributes to its global transport (Chen et al. 2014). Within aquatic and terrestrial habitats, Hg can be found in various forms, but most studies focus on inorganic Hg and MeHg. The most toxic form of Hg, MeHg, is commonly produced by interactions between anaerobic sulfur-reducing bacteria and inorganic Hg (Klaus et al. 2016). Bioaccumulation of MeHg is facilitated by dietary exposure, with higher Hg burdens reported in top trophic predators (Scheuhammer et al.

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