Effects of nitrate and atrazine on larval development and sexual differentiation in the northern leopard frog <i>Rana pipiens</i>

Orton, Frances; Carr, James A.; Handy, Richard D.

doi:10.1897/05-136r.1

Cited by 94 publications

(92 citation statements)

References 51 publications

(96 reference statements)

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“…Our study also demonstrates that nitrate-exposed X. laevis exhibit altered ovarian follicle diameters. These results are similar to altered ovarian follicles reported for larval Leopard Frogs exposed to nitrate (Orton et al, 2006).…”

Section: Resultssupporting

confidence: 90%

“…Nitrate exposure is also associated with gonadal atrophy, altered sperm morphology, and decreased sperm count in rodents (Pant and Srivastava, 2002), in addition to suppressed Leydig cell activity and reduced sperm motility in bulls (Zraly et al, 1997). Larval anurans exposed to nitrate exhibit altered sperm cell ratios and ovarian follicle maturation (Orton et al, 2006). In accord with these observations, in this study we hypothesized that exposure to environmentally relevant nitrate could alter ovarian steroid synthesis and follicle size in a model frog species, Xenopus laevis.…”

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confidence: 77%

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Altered Ovarian Steroids in Xenopus Laevis Exposed to Environmentally Relevant Concentrations of Nitrate

Barbeau

Guillette

2007

Journal of Herpetology

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ABSTRACT.-Contamination of aquatic ecosystems with anthropogenic sources of nitrate is of increasing concern. Anurans are especially at risk for overexposure to nitrate because they occupy aquatic environments during embryonic, larval, and adult stages. Whereas there have been numerous studies examining the effect of nitrate on frog eggs and tadpoles, the effects of nitrate on adult frogs have been largely neglected. In this study, we examined whether brief exposure to environmentally relevant concentrations of aquatic nitrate influenced ovarian steroid synthesis and ovarian follicle size in adult African Clawed Frogs (Xenopus laevis). We exposed frogs for seven days to nitrate at concentrations of 24.8 or 49.5 mg/l in order to simulate a pulse of nitrate exposure. Relative to controls, nitrate-exposed frogs exhibited suppressed ex vivo synthesis of testosterone and estrogen. Follicles from nitrate-exposed frogs also exhibited an increased stage-4 diameter at both nitrate concentrations and a decreased stage-5 and -6 diameter at the highest nitrate concentration. These results indicate that anuran ovarian steroidogenesis and follicle size are modified by even a brief exposure to environmentally relevant concentrations of nitrate. Contamination ;of aquatic ecosystems by anthropogenic sources of nitrate has become an increasing global concern with respect to the health of humans and wildlife (Fried, 1991;Guillette and Edwards, 2005). Nitrate contamination of aquatic habitats occurs primarily through human activities in agricultural and urban areas, and in North American rivers, streams, and lakes, nitrate concentrations range from 1 mg/l to over 100 mg/l nitrate-as-nitrogen (Rouse et al., 1999). Within the United States, agricultural nitrogen contributions have increased 20-fold in the past 50 years, because of poorly regulated runoff of nitrogen-based fertilizers and animal wastes (Puckett, 1995;Rouse et al., 1999). Within urban areas, nitrate infiltrates aquatic ecosystems primarily through release of industrial and wastewater effluents from treatment plants, runoff of fertilizer applied to lawns and golf courses, and air pollution from the burning of fossil fuels (Rouse et al., 1999). In North America, fertilizers applied adjacent to waterways, coupled with spring rainstorms, contribute to a pulse of nitrate entering aquatic habitats that coincides with the breeding season of many amphibians (Rouse et al., 1999).Nitrate is highly soluble in water and, if ingested or absorbed transdermally, is readily transported across the epithelium of the small intestine (Ellis et al., 1998;Iizua et al., 1999). Numerous investigations of tadpoles exposed to environmentally relevant concentrations of nitrate have demonstrated altered behaviors (Hecnar, 1995;, movement patterns (Xu and Oldham, 1997), growth rates, development (Baker and Waights, 1993, 1994;Edwards et al., 2006), gonadal morphology (Orten et al., 2006), and mortality rates Smith et al., 2005Smith et al., , 2006. However, the effects of nitrate on endocrine func...

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Section: Resultssupporting

confidence: 90%

mentioning

confidence: 77%

Altered Ovarian Steroids in Xenopus Laevis Exposed to Environmentally Relevant Concentrations of Nitrate

Barbeau

Guillette

2007

Journal of Herpetology

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“…and higher), atrazine causes a decrease in the gonadal volume and germ cells in exposed Xenopus laevis larvae (Tavera-Mendoza et al, 2002a;TaveraMendoza et al, 2002b). Further, atrazine induces hermaphroditism in exposed X. laevis frogs (Carr et al, 2003;Hayes et al, 2002a;Hayes et al, 2002b;Hayes et al, 2006b) and testicular oogenesis in Ranid frogs exposed as larvae (Hayes et al, 2002c;Hayes et al, 2006b;Orton et al, 2006). Sexual abnormalities are also associated with atrazine contamination in free-ranging amphibians in the wild (Hayes et al, 2002b;Hayes et al, 2002c) and where animals are exposed in mesocosm studies (Langlois et al, 2009).…”

Section: Environmental Pollutants Affect Recruitmentmentioning

confidence: 99%

The cause of global amphibian declines: a developmental endocrinologist's perspective

Hayes

Falso

Gallipeau

et al. 2010

Journal of Experimental Biology

356

228

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SummaryGreater than 70% of the world's amphibian species are in decline. We propose that there is probably not a single cause for global amphibian declines and present a three-tiered hierarchical approach that addresses interactions among and between ultimate and proximate factors that contribute to amphibian declines. There are two immediate (proximate) causes of amphibian declines: death and decreased recruitment (reproductive failure). Although much attention has focused on death, few studies have addressed factors that contribute to declines as a result of failed recruitment. Further, a great deal of attention has focused on the role of pathogens in inducing diseases that cause death, but we suggest that pathogen success is profoundly affected by four other ultimate factors: atmospheric change, environmental pollutants, habitat modification and invasive species. Environmental pollutants arise as likely important factors in amphibian declines because they have realized potential to affect recruitment. Further, many studies have documented immunosuppressive effects of pesticides, suggesting a role for environmental contaminants in increased pathogen virulence and disease rates. Increased attention to recruitment and ultimate factors that interact with pathogens is important in addressing this global crisis.

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“…Atrazine seems to be most potent in amphibians, where it is active at levels as low as 0.1 ppb (6)(7)(8)(9)(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)(8)(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).…”

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confidence: 99%

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.

499

299

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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...

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Effects of nitrate and atrazine on larval development and sexual differentiation in the northern leopard frog Rana pipiens

Cited by 94 publications

References 51 publications

Altered Ovarian Steroids in Xenopus Laevis Exposed to Environmentally Relevant Concentrations of Nitrate

Altered Ovarian Steroids in Xenopus Laevis Exposed to Environmentally Relevant Concentrations of Nitrate

The cause of global amphibian declines: a developmental endocrinologist's perspective

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

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