Effects of mercury on behavior and performance of northern two-lined salamanders (Eurycea bislineata)
Introduction
Mercury (Hg) is a widespread contaminant of considerable ecological concern due to its toxicity to fish and wildlife (e.g., Scheuhammer et al., 2007, Wolfe et al., 1998) and its tendency to biomagnify in ecosystems (e.g., Hall et al., 1998). Although Hg occurs naturally, environmental occurrence and concentrations have increased due to redistribution associated with industrial processes (Fitzgerald et al., 1998). Mercury occurs in both inorganic and organic forms, but it is the highly toxic methylmercury (MeHg) that efficiently bioaccumulates in organisms (Hill et al., 1996, Watras and Bloom, 1992) and biomagnifies in food webs (Hall et al., 1998). Methylmercury is primarily synthesized by anaerobic sulfate-reducing bacteria in marine and freshwater sediments (Gilmour et al., 1992, Benoit et al., 1998), which make fauna associated with these environments particularly susceptible to contamination. The adverse effects of Hg exposure are often associated with its neurotoxicity; however, Hg has also been linked to immune suppression, endocrine disruption, physical malformations, and mortality in organisms (Eisler, 2006, Scheuhammer et al., 2007, Tan et al., 2009, Wada et al., 2009, Weiner and Spry, 1996, Wolfe et al., 1998).
Behavior is the action exhibited by an organism in response to stimuli, and it is the direct manner by which an organism interacts with its environment. Behavioral changes result from interactions of environmental, chemical, and neurological variables between the organism and its surroundings and can be advantageous, deleterious, or have no effect on the individual’s well-being. Exposure to certain environmental contaminants, especially neurotoxicants such as Hg, can promote the expression or suppression of behaviors and affect performance (Henry and Atchison, 1991), the proficiency with which an organism executes a behavior. The neuron degeneration caused by Hg (Sakamoto et al., 1998) suggests that the metal could potentially disrupt the brain’s ability to effectively control motor functions. The resulting behavioral effects may inhibit an organism’s ability to capture prey, avoid predators, or successfully compete with others (Little et al., 1990, Walker et al., 2005). For example, a study of mosquitofish (Gambusia affinis) aqueously exposed to mercurial chloride demonstrated altered swimming activity and decreased swimming speed (Jakka et al., 2007). Similarly, Alvarez et al. (2006) noted concentration-dependent effects of maternally-transferred MeHg in larval Atlantic croaker (Micropogonias undulatus), including decreased response speed and increased response time to a vibratory stimulus. Thus, functional impairments, such as altered prey capture ability and reduced performance in individuals, could theoretically reduce fitness, lower recruitment, and even cause population declines.
Many studies regarding the effects of Hg have focused on fish, birds, and mammals (Eisler, 2006, Scheuhammer et al., 2007, Wolfe et al., 1998), but amphibians have received little attention apart from measuring and reporting Hg-tissue concentrations (e.g., Bank et al., 2007, Bergeron et al., 2010a, Eisler, 2006, Linder and Grillitsch, 2000). However, the life history traits and ecological strategies of many amphibian species, such as a complex lifecycle with an aquatic larval stage, omnivorous and carnivorous diets, and use of a wide range of habitats, make them particularly appropriate for studying the effects of Hg contamination on wildlife (Hopkins, 2007). Amphibians can also have important roles in many ecosystems. In certain areas, amphibians represent a critical energy source to predators due to their high biomass, especially in eastern forests of the United States (Burton and Likens, 1975). Due to their abundance and life history, amphibians with complex lifecycles often link trophic levels and facilitate the transfer of nutrients and energy between aquatic and terrestrial habitats (Beard et al., 2002, Regester et al., 2006, Wyman, 1998). Additionally, amphibians are capable of using more of their energy intake for tissue production than endotherms at similar trophic levels (Burton and Likens, 1975, Grayson et al., 2005), increasing their potential to accumulate high Hg concentrations in their tissue (Unrine et al., 2007). Finally, in the last 30 years, biologists have observed marked declines in amphibian populations, putting many of them at greater risk of extinction than birds or mammals (Stuart et al., 2004). While past research indicates that habitat loss and disease are causing many declines, anthropogenic contaminants, like Hg, may also contribute (Beebee and Griffiths, 2005).
Our objective in this study was to determine the effects of Hg contamination along the South River, VA, USA on the performance and behavior of northern two-lined salamanders (Eurycea bislineata). We chose northern two-lined salamanders for this study because they have been shown to have the highest total Hg (THg) concentrations of the three amphibian species studied on the South River, and also have some of the highest THg concentrations (up to 5,785 ng/g, dry wt prior to this study) reported in the literature for amphibians (Bergeron et al., 2010a). To accomplish our objective, we used two experiments to determine whether northern two-lined salamanders from the Hg-contaminated portion of the South River would exhibit reduced locomotor performance and reduced prey capture ability when compared with conspecifics from an upstream, reference portion of the river.
Section snippets
Site description
The South River, VA, USA is a tributary of the Shenandoah River and has a history of anthropogenic Hg contamination from an acetate fiber manufacturing plant in Waynesboro, VA that used Hg in its manufacturing processes from 1929 to 1950 (Carter, 1977). Mercury concentrations in the river currently remain elevated (Southworth et al., 2004) and continue to contaminate wildlife species (Bergeron et al., 2007, Bergeron et al., 2010a, Brasso and Cristol, 2008, Cristol et al., 2008, Wada et al., 2009
Results
Average THg tissue concentrations (Fig. 1) for northern two-lined salamanders collected from contaminated sites were ∼17.5 times higher than those from reference sites (4,519 ± 348 and 256 ± 26 ng/g, respectively) (Z = −4.88, P < 0.001). Using the percent MeHg (61.2%) found by Bergeron et al. (2010b) for northern two-lined salamanders in a previous study at the South River, the average THg concentrations are equivalent to 2,766 and 157 ng/g MeHg (Fig. 1) at the contaminated and reference sites,
Discussion
Anthropogenic contaminants are suspected contributors to global amphibian declines but the ways in which they may contribute to these declines is poorly understood (Beebee and Griffiths, 2005). The purpose of our study was to examine the potential impacts of Hg contamination on amphibians in light of these declines. While other studies have identified the tendency for Hg to accumulate in amphibian tissues (e.g., Bank et al., 2007, Bergeron et al., 2010a, Eisler, 2006, Linder and Grillitsch, 2000
Acknowledgments
Many thanks to D. Cristol for assistance with Hg analyses, M. Hepner and M. McCaleb for their laboratory and collection assistance, and to K. Grayson for collecting animals for pilot studies. This research would not have been possible without the support from J. Schmerfeld (U.S. Fish & Wildlife), the South River Science Team, and the cooperation of the landowners along the South River and the Waynesboro Parks and Recreation Department. Financial support was provided by E.I. DuPont de Nemours
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Present address: University of California, Davis, Department of Wildlife, Fish, and Conservation Biology, One Shields Ave, Davis, CA 95616, USA.