Suburbanization feminizes frog offspring sex ratios

In September Proceedings of the National Academy of Sciences published an article called “Suburbanization, estrogen contamination, and sex ratio in wild amphibian populations”. We asked one of the authors, Max Lambert from Yale University, to comment on this study.

The Study

We studied a set of 21 small ponds in southwestern Connecticut. Using land cover data derived from satellite imagery, we were able to classify our ponds along a suburban gradient. This means some of our ponds were entirely surrounded by forest cover, others by dense suburban neighborhoods, and everything in between. Our goal was to understand whether suburban land use influence sexual development in young frogs and whether water contamination was in anyway correlated with effects in the frogs. We sampled young frogs at metamorphosis, when they had all four legs and their tadpole tail was shrinking; this stage of frog development is very similar to birth in humans.

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To our surprise sex ratios (the proportion of males and females in a sample) were heavily male-biased in forested ponds – forested pond frog sex ratios were 2/3 male. Even more remarkable was that sex ratios became increasingly-feminized and contained proportionally more females as ponds became more and more impacted by suburban land use. The male-biased sex ratios in forested ponds are particularly interesting because it suggests that sex reversal may be happening in natural systems in the absence of human-made chemicals. Furthermore, that increasing human land use intensity is linked to proportionally more females in frog offspring cohorts implies that our everyday activities can cause frog sexual development to deviate from normal. This is really the first example of sex ratio variation of this sort in an amphibian and provides us with evidence that sexual development and sex reversal in amphibians are malleable to environmental conditions.

Parallel to this, we analyzed a variety of chemicals in these ponds. We found that as ponds became increasingly impacted by suburbanization they were also increasingly contaminated by a set of contaminants known as estrogenic endocrine disrupting chemicals. Specifically, we found a set of “classic” estrogens, like estrone, which are made by a variety of organisms, including people. We also found a diversity of phytoestrogens; these chemicals are made by plants and act like estrogen in animals. Interestingly, the diversity of phytoestrogens we found in our ponds was correlated with the amount of suburban landscaping (lawns, gardens, etc.) surrounding a pond. This result suggests that the plants we landscape in our backyards may be making chemicals that are contributing to feminizing frog populations. However, the high diversity of chemicals we found in our ponds suggests that there are many sources of estrogenic contaminants in these ponds. These might possibly include leaky septic systems or road runoff.

Background

Feminizing endocrine disruption in wildlife really has a history grounded in two systems. The first are fish downstream from wastewater treatment facilities (WWTF). Numerous studies around the world have shown that WWTFs often do not remove many of our pharmaceuticals before water is put back into a stream. Wild male fish exposed to these pharmaceuticals frequently are feminized and are less capable of reproduction. Secondly, in frogs, a large body of work has focused on understanding how pesticides, and Atrazine in particular, feminize male frogs in agricultural landscapes. Our lab became interested in this work almost a decade ago but more so from a landscape ecology perspective. My advisor, Dr. David Skelly, was interested in which human land uses were hotspots of endocrine disruption in frogs. The answer was very clear – the suburbs. Our lab showed that, basically wherever you go in suburban neighborhoods, you will find feminized males. You will never find these types of males in natural, forested ponds.

Future Directions

This work has shown us that the scientific community actually knows very little about sex reversal in amphibians, both in natural environments as well as human-dominated landscapes. Whether being a male or female is relatively fluid for frogs or whether it takes a big chemical dose to transform a male into a female, or a female into a male, is predominantly unknown in wild frog populations. To really understand the degree and importance of toxicological effects on sexual development, we need to have a better understanding of natural, baseline sexual development in frogs. Our work now is going in this direction; we are trying to develop a deeper understanding of normal, natural sexual development and sex reversal patterns in frogs and how people are changing these dynamics.