Do hormone‐modulating chemicals impact on reproduction and development of wild amphibians?

Abstract

Globally, amphibians are undergoing a precipitous decline. At the last estimate in 2004, 32% of the approximately 6000 species were threatened with extinction and 43% were experiencing significant declines. These declines have been linked with a wide range of environmental pressures from habitat loss to climate change, disease and pollution. This review evaluates the evidence that endocrine-disrupting contaminants (EDCs) -pollutants that affect hormone systems -are impacting on wild amphibians and contributing to population declines. The review is limited to anurans (frogs and toads) as data for effects of EDCs on wild urodeles (salamanders, newts) or caecilians (limbless amphibians) are extremely limited. Evidence from laboratory studies has shown that a wide range of chemicals have the ability to alter hormone systems and affect reproductive development and function in anurans, but for the most part only at concentrations exceeding those normally found in natural environments. Exceptions can be found for exposures to the herbicide atrazine and polychlorinated biphenyls in leopard frogs (Rana pipiens) and perchlorate in African clawed frogs (Xenopus laevis). These contaminants induce feminising effects on the male gonads (including 'intersex' -oocytes within testes) at concentrations measured in some aquatic environments. The most extensive data for effects of an EDC in wild amphibian populations are for feminising effects of atrazine on male gonad development in regions across the USA. Even where strong evidence has been provided for feminising effects of EDCs, however, the possible impact of these effects on fertility and breeding outcome has not been established, making inference for effects on populations difficult. Laboratory studies have shown that various chemicals, including perchlorate, polychlorinated biphenyls and bromodiphenylethers, also act as endocrine disrupters through interfering with thyroid-dependent processes that are fundamental for amphibian metamorphosis. Perchlorate has also been shown to induce these effects in wild anuran populations from perchlorate-contaminated environments. Overall, the published data available suggest that some health effects observed in wild anuran populations, most notably intersex, likely have a chemical aetiology; however they derive only from very few anuran species and for a few pesticides at field sites in the USA. To understand better the impacts of EDCs on wild anuran populations, as well as other amphibian groups, assessment of fertility in exposed animals are required. Development of non-destructive biomarkers that are indicative of specific EDC-effect mechanisms are also needed to allow the study of vulnerable populations. This will help to distinguish the effects of EDCs from other environmental and/or genetic influences on development and reproduction.

Sex Reversal in Reptiles: Reproductive Oddity or Powerful Driver of Evolutionary Change?

“…Hormonal manipulation and exposure to exogenous chemicals can cause sex reversal in amphibians with sex chromosomes [Dournon et al, 1990;Orton and Tyler, 2015], and similar manipulations have been conducted with TSD reptiles [Bull et al, 1988;Belaid et al, 2001;Warner and Shine, 2008;Mizoguchi and Valenzuela, 2016] reversing sex from that expected given the temperature of incubation. However, the relevance of these studies to what happens in the wild remains the subject of some conjecture.…”

Climate change and pollution speed declines in zebrafish populations

“…However, in lizards (17,18), fish (21), and some amphibians (22), temperature elevation tends to induce male development and male-biased sex ratios can dramatically reduce population fitness (23,24). Sexual differentiation in these animals is also strongly influenced by chemicals that disrupt hormone systems (25)(26)(27)(28). Some endocrine disrupting chemicals (EDCs) are highly potent pollutants, and exposure concentrations occurring in natural surface waters have been shown to affect reproductive development negatively in reptiles (29), amphibians (28), and fish (30,31).…”

“…Sexual differentiation in these animals is also strongly influenced by chemicals that disrupt hormone systems (25)(26)(27)(28). Some endocrine disrupting chemicals (EDCs) are highly potent pollutants, and exposure concentrations occurring in natural surface waters have been shown to affect reproductive development negatively in reptiles (29), amphibians (28), and fish (30,31).…”

The plasticizer bisphenol A affects somatic and sexual development, but differently in pipid, hylid and bufonid anurans

“…Due to their highly permeable skin and, in most species, aquatic larval phase, dissolved chemicals can easily enter the body of amphibians and impair their somatic and sexual development by interference with the organisms' hormonal control. In addition, most amphibians are terrestrial as adults, and are thus also potential recipients of EDCs found in the terrestrial environment (Bhandari et al, 2015;Kloas, 2002;Orton and Tyler, 2014). Several studies testing effects of BPA on the somatic development of amphibians have been conducted and multiple negative outcomes were observed.…”