Black arrowheads in A and B show boundaries of nuptial pads.
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Note the reduced nuptial pads in the atrazine-exposed male (B).
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( A and B) Forearms, showing nuptial pads from control ( A) and atrazine-exposed males ( B). Atrazine-demasculinized male morphology as shown in the nuptial glands and the larynx. These ZZ females expressed gonadal aromatase, as did true ZW females ( n = 4, from our stock colony), but ZZ males ( n = 8, control or treated) did not ( Fig. Furthermore, atrazine-induced females lacked the DM-W further confirming that these atrazine-induced females were indeed chromosomal males ( Fig. The resulting larvae were all male when raised to metamorphosis and sampled ( n = 100), confirming that atrazine-induced females were, in fact, chromosomal males. To date, two atrazine-induced females have been maintained, mated with control males ( Fig. Upon dissection of two of the apparent females and laparotomy in another two, we confirmed that animals with cloacal labia were indeed females from the present study, on the basis of the presence of ovaries ( Fig. The other 10% of atrazine-exposed animals ( n = 4) lacked visible nuptial pads on the forearms and had protruding cloacal labia, typical of females ( Fig. Results Feminization.Īll of the control animals reared to sexual maturity ( n = 40) were males, on the basis of external morphology, whereas only 90% of the atrazine-treated animals (36 of 40) appeared male at sexual maturity (on the basis of the presence of keratinized nuptial pads on the forearms and the absence of cloacal labia). We examined sex ratios, testosterone levels, sexual dimorphism, reproductive behaviors, and fertility in males exposed to 2.5 ppb atrazine throughout the larval period and for up to 3 years after metamorphosis. As a result, all hermaphrodites and females observed are ensured to be genetic males that have been altered by endocrine disruption. The advantage of using this population is that 100% of the animals tested were genetic males. In the present study, we examined the long-term effects of atrazine exposure on reproductive development and function in an all-male population of African clawed frogs ( Xenopus laevis), generated by crossing ZZ females (sex-reversed genetic males) to ZZ males ( SI Materials and Methods). 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).ĭespite 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 been unexplored. 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). Atrazine seems to be most potent in amphibians, where it is active at levels as low as 0.1 ppb ( 6– 10). 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). The present findings exemplify the role that atrazine and other endocrine-disrupting pesticides likely play in global amphibian declines. These data are consistent with effects of atrazine observed in other vertebrate classes.
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Atrazine-exposed males suffered from depressed testosterone, decreased breeding gland size, demasculinized/feminized laryngeal development, suppressed mating behavior, reduced spermatogenesis, and decreased fertility. Ten percent of the exposed genetic males developed into functional females that copulated with unexposed males and produced viable eggs. Atrazine-exposed males were both demasculinized (chemically castrated) and completely feminized as adults. The present study demonstrates the reproductive consequences of atrazine exposure in adult amphibians. Previous studies showed that atrazine adversely affects amphibian larval development.
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Atrazine is also a potent endocrine disruptor that is active at low, ecologically relevant concentrations. As a result, atrazine is the most commonly detected pesticide contaminant of ground, surface, and drinking water. The herbicide atrazine is one of the most commonly applied pesticides in the world.