FROGS, SEX, AND ESTROGEN: RELATIONSHIPS WITH TRACE ELEMENTS AND SUBURBANIZATION

Urban land use is increasing globally. Suburbanization is of particular interest because its growth is outpacing that of cities, and suburban neighborhoods have previously been shown to have higher levels of contamination than other land uses. Of increasing concern are endocrine disrupting chemicals (EDCs), compounds which are known to alter hormone function and regulation in vertebrates. Prior work has shown that endocrine disruption, as measured by the incidence of testicular deformities in frogs, is higher in suburban neighborhoods as compared to a variety of other land uses, implicating relatively high loads of EDCs. Typically, research has focused on organic EDCs, both natural and synthetic; however, there is laboratory evidence that some metals (termed metalloestrogens) have estrogen-like effects in humans and animals. Here we surveyed a spectrum of organic EDCs as well trace elements along a land-use gradient of undeveloped, forested wetlands to suburban ponds surrounded by highly-developed areas. We also sampled developing green frogs (Rana clamitans) along this gradient and measured frog estrogen levels and the sex ratio (proportion female) within each developing cohort.

Our results show mixed effects of suburbanization on frog biology. We found that both the frog offspring sex ratio as well as the number of organic, estrogenic chemicals increased with increasing suburbanization. The concentration of known metalloestrogens was also much higher in suburban ponds relative to forest ponds. We also found that variation in estrogen levels (E2) among frogs within a pond showed strong negative correlations with trace elements. Specifically, as concentrations of antimony, a known metalloestrogen, increased in a po­­nd, variation in E2 for females decreased. In male frogs, variation in E2 decreased as a function of multiple collinear trace elements, many of which are rare earth elements (REEs). Interestingly, these relationships between frog estrogen levels and trace elements do not follow patterns of anthropogenic land use. Our work highlights the importance of evaluating trace elements as relevant hormonally-active chemicals and the need to study both natural as well as anthropogenic variation in aqueous geochemistry.