Reproduction, Embryonic Development, and Maternal Transfer of Contaminants in the Amphibian Gastrophryne Carolinensis
Hopkins, William Alexander, DuRant, Sarah Elizabeth, Staub, Brandon Patrick, Rowe, Christopher Lee, Jackson, Brian Phillip, Environmental Health Perspectives
Although many amphibian populations around the world are declining at alarming rates, the cause of most declines remains unknown. Environmental contamination is one of several factors implicated in declines and may have particularly important effects on sensitive developmental stages. Despite the severe effects of maternal transfer of contaminants on early development in other vertebrate lineages, no studies have examined the effects of maternal transfer of contaminants on reproduction or development in amphibians. We examined maternal transfer of contaminants in eastern narrow-mouth toads (Gastrophryne carolinensls) collected from a reference site and near a coal-burning power plant. Adult toads inhabiting the industrial area transferred significant quantities of selenium and strontium to their eggs, but Se concentrations were most notable (up to 100 [micro]g/g dry mass). Compared with the reference site, hatching success was reduced by 11% in clutches from the contaminated site. In surviving larvae, the frequency of developmental abnormalities and abnormal swimming was 55-58% higher in the contaminated site relative to the reference site. Craniofacial abnormalities were nearly an order of magnitude more prevalent in hatchlings from the contaminated site: When all developmental criteria were considered collectively, offspring from the contaminated site experienced 19% lower viability. Although there was no statistical relationship between the concentration of Se or Sr transferred to eggs and any measure of offspring viability, our study demonstrates that maternal transfer may be an important route of contaminant exposure in amphibians that has been overlooked. Key words: amphibian, coal combustion, development, embryo, maternal transfer, mercury, reproduction, selenium, strontium. doi:10.1289/ehp.8457 available via http://dx.doi.org/ [Online 8 December 2005]
Amphibian populations around the world are declining at alarming rates, but the causes of most declines are unknown. Habitat destruction and alteration are most likely the largest contributors to population declines, but other factors such as introduction of exotic species, emerging diseases, global climate change, and environmental contamination likely influence population viability (Collins and Storfer 2003; Stuart et al. 2004). The importance of environmental contamination in population declines is poorly understood, partly because of the dearth of information on effects of contaminants on responses of individuals (e.g., reproduction) that directly influence the viability of natural populations.
Exposure of sensitive embryonic life stages to contaminants may be an important mechanism of impaired reproductive success in amphibians. Developmental pathways in embryonic amphibians can be altered when embryos are exposed to contaminants via two primary mechanisms: uptake from their surroundings (water) and transfer from females to offspring. Most of what is currently known about the effects of contaminants on amphibian development is derived from studies in which embryos are exposed via water. In fact, aqueous exposure has formed the foundation for the only widely accepted standardized amphibian toxicity test (frog embryo teratogenesis assay-Xenopus) [American Society for Testing and Materials (ASTM) 1998; Bantle et al. 1991]. In contrast, maternal transfer has been an understudied mechanism of reproductive impairment in amphibians. One previous study demonstrated that amphibians partition significant quantities of cadmium in reproductive tissues (in follicles and eggs before oviposition), suggesting the potential for maternal transfer to offspring (Linder et al. 1998). Kadokami et al. (2004) went a step further when they demonstrated that frogs can maternally transfer organic contaminants to their eggs. However, no studies have examined the effect of maternal transfer on reproduction and development in amphibians, despite well-known effects of maternally derived contaminants in all other major vertebrate lineages (e. …