Low Levels of the Herbicide Atrazine Alter Sex Ratios and Reduce Metamorphic Success in
            <i>Rana pipiens</i>
            Tadpoles Raised in Outdoor Mesocosms

Langlois, Valérie S.; Carew, Amanda C.; Pauli, Bruce D.; Wade, Michael G.; Cooke, Gerard M.; Trudeau, Vance L.

doi:10.1289/ehp.0901418

Cited by 76 publications

(61 citation statements)

References 51 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Furthermore, we showed that feminization is persistent and complete, resulting in reproductively functional females capable of producing viable eggs. Together, the present data and these three similar reports (5,39,40) suggest that sex-reversal by atrazine (complete feminization of genetic males) is not a species-specific effect but rather one that occurs across nonamniote vertebrate classes.…”

Section: Discussionsupporting

confidence: 83%

Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis)

Hayes

Khoury

Narayan

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

526

307

View full text Add to dashboard Cite

The herbicide atrazine is one of the most commonly applied pesticides in the world. As a result, atrazine is the most commonly detected pesticide contaminant of ground, surface, and drinking water. Atrazine is also a potent endocrine disruptor that is active at low, ecologically relevant concentrations. Previous studies showed that atrazine adversely affects amphibian larval development. The present study demonstrates the reproductive consequences of atrazine exposure in adult amphibians. Atrazineexposed males were both demasculinized (chemically castrated) and completely feminized as adults. Ten percent of the exposed genetic males developed into functional females that copulated with unexposed males and produced viable eggs. Atrazineexposed males suffered from depressed testosterone, decreased breeding gland size, demasculinized/feminized laryngeal development, suppressed mating behavior, reduced spermatogenesis, and decreased fertility. These data are consistent with effects of atrazine observed in other vertebrate classes. The present findings exemplify the role that atrazine and other endocrine-disrupting pesticides likely play in global amphibian declines.A trazine is one of the most widely used pesticides in the world. Approximately 80 million pounds are applied annually in the United States alone, and atrazine is the most common pesticide contaminant of ground and surface water (1). Atrazine can be transported more than 1,000 km from the point of application via rainfall and, as a result, contaminates otherwise pristine habitats, even in remote areas where it is not used (2, 3). In fact, more than a half million pounds of atrazine are precipitated in rainfall each year in the United States (2).In addition to its persistence, mobility, and widespread contamination of water, atrazine is also a concern because several studies have shown that atrazine is a potent endocrine disruptor active in the ppb (parts per billion) range in fish (4, 5), amphibians (6-12), reptiles, and human cell lines (5, 13-15), and at higher doses (ppm) in reptiles (16-18), birds (19), and laboratory rodents (20-28). Atrazine seems to be most potent in amphibians, where it is active at levels as low as 0.1 ppb (6-10). Although a few studies suggest that atrazine has no effect on amphibians under certain laboratory conditions (29,30), in other studies, atrazine reduces testicular volume; reduces germ cell and Sertoli cell numbers (11); induces hermaphroditism (6, 8, 10); reduces testosterone (10); and induces testicular oogenesis (7-9, 31). Furthermore, atrazine contamination is associated with demasculinization and feminization of amphibians in agricultural areas where atrazine is used (32) and directly correlated with atrazine contamination in the wild (7,9,33,34).Despite the wealth of data from larvae and newly metamorphosed amphibians, the ultimate impacts of atrazine's developmental effects on reproductive function and fitness at sexual maturity, which relate more closely to population level effects and amphibian declines, have b...

show abstract

Section: Discussionsupporting

confidence: 83%

Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis)

Hayes

Khoury

Narayan

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

526

307

View full text Add to dashboard Cite

show abstract

“…This result, coupled with studies illustrating that amphibian sex differentiation is sensitive to estrogen exposure in the laboratory (8,12,15,16), challenges the assumption that amphibian sex determination is strictly genetic (14) and implies a potential role for environmental sex modification. Offspring sex ratio is generally poorly studied in metamorphosing amphibians from wild populations, though it is commonly understood that amphibians have genetic sex determination (14).…”

Section: Discussionmentioning

confidence: 96%

“…Offspring sex ratio is generally poorly studied in metamorphosing amphibians from wild populations, though it is commonly understood that amphibians have genetic sex determination (14). Although laboratory studies indicate that amphibian sex ratios can be environmentally manipulated (8,12), these prior results provide no indication of normal sex ratio variation in wild populations from different environments. Limited evidence from a single natural frog population indicates that normal metamorph sex ratios can sometimes be skewed toward one sex (17).…”

Section: Discussionmentioning

confidence: 99%

“…S1), and focused on sex ratios of green frogs (R. clamitans), which inhabit both environments and were previously evaluated for evidence of endocrine disruption (6, 7). Offspring sex ratio is an established metric of endocrine disruption (8,12) and is ecologically relevant (13). Here, we address whether sex ratio in cohorts of metamorphosing green frogs varies with landscape structure surrounding ponds.…”

mentioning

confidence: 99%

“…Wild amphibians show evidence (such as testicular oocytes) of feminizing endocrine disruption in human-modified environments (2)(3)(4)(5)(6)(7). With few exceptions (6,7), research on amphibians has focused on agricultural landscapes (2,4,5) and the effects of pesticides such as atrazine (2,8). In parallel, endocrine disruption in fish has been observed in the context of chemical gradients associated with sources of endocrine disrupting chemicals (EDCs) such as municipal wastewater treatment facility discharges (9)(10)(11).…”

mentioning

confidence: 99%

See 2 more Smart Citations

Suburbanization, estrogen contamination, and sex ratio in wild amphibian populations

Lambert

Giller

Barber

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Research on endocrine disruption in frog populations, such as shifts in sex ratios and feminization of males, has predominantly focused on agricultural pesticides. Recent evidence suggests that suburban landscapes harbor amphibian populations exhibiting similar levels of endocrine disruption; however the endocrine disrupting chemical (EDC) sources are unknown. Here, we show that sex ratios of metamorphosing frogs become increasingly female-dominated along a suburbanization gradient. We further show that suburban ponds are frequently contaminated by the classical estrogen estrone and a variety of EDCs produced by plants (phytoestrogens), and that the diversity of organic EDCs is correlated with the extent of developed land use and cultivated lawn and gardens around a pond. Our work also raises the possibility that trace-element contamination associated with human land use around suburban ponds may be contributing to the estrogenic load within suburban freshwaters and constitutes another source of estrogenic exposure for wildlife. These data suggest novel, unexplored pathways of EDC contamination in human-altered environments. In particular, we propose that vegetation changes associated with suburban neighborhoods (e.g., from forests to lawns and ornamental plants) increase the distribution of phytoestrogens in surface waters. The result of frog sex ratios varying as a function of human land use implicates a role for environmental modulation of sexual differentiation in amphibians, which are assumed to only have genetic sex determination. Overall, we show that endocrine disruption is widespread in suburban frog populations and that the causes are likely diverse.A mphibians are a model animal system for studying endocrine disruption in nature (1). Wild amphibians show evidence (such as testicular oocytes) of feminizing endocrine disruption in human-modified environments (2-7). With few exceptions (6, 7), research on amphibians has focused on agricultural landscapes (2, 4, 5) and the effects of pesticides such as atrazine (2,8). In parallel, endocrine disruption in fish has been observed in the context of chemical gradients associated with sources of endocrine disrupting chemicals (EDCs) such as municipal wastewater treatment facility discharges (9-11). These studies imply that endocrine disruption in aquatic systems is caused predominantly by industrial-or municipalscale activities. However, recent work has revealed that suburban neighborhoods also may be hotspots for endocrine disruption, and green frogs [Rana (Lithobates) clamitans] from "backyard ponds" have been reported (6, 7) to exhibit higher frequencies of feminizing endocrine disruption (testicular oocytes in males) than frogs from other land uses (forest, agricultural, and urban). Endocrine disruption appears to be a ubiquitous phenomenon in suburban ponds, with testicular oocytes observed in male green frogs at all 34 suburban ponds studied to date (6, 7). The causes of endocrine disruption in suburban landscapes have not yet been studied. Although some ...

show abstract

Endocrine Disruption in Wildlife: Background, Effects, and Implications

Vethaak¹,

Legler²

2013

Endocrine Disrupters

View full text Add to dashboard Cite

Low Levels of the Herbicide Atrazine Alter Sex Ratios and Reduce Metamorphic Success in Rana pipiens Tadpoles Raised in Outdoor Mesocosms

Cited by 76 publications

References 51 publications

Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis)

Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis)

Suburbanization, estrogen contamination, and sex ratio in wild amphibian populations

Endocrine Disruption in Wildlife: Background, Effects, and Implications

Contact Info

Product

Resources

About