For many decades, there has been concern about the effects of environmental contaminants on the health and persistence of wildlife populations. Prior to work over the last 10-15 years, the vast majority of these studies examined the lethal consequences of exposure, or they focused on the induction of cancer or major birth defects. Although these endpoints are still critical in the study of toxicology, a growing collection of studies examining diverse wildlife species demonstrates that additional adverse outcomes can be produced in wildlife as a result of exposure to environmental contaminants. A number of these abnormalities have been attributed to the disruption of endocrine signaling. Below, we examine a few of the many examples of endocrine disruption in wildlife.
Fish, Vitellogenesis, and Sewage
In the 1990s, reports were published documenting that male fish living below sewage outfalls in Europe, Great Britain, North America, and Japan had elevated plasma concentrations of the yolk protein vitellogenin. Vitellogenin is normally synthesized in the liver of the female following stimulation by elevated plasma estrogens of ovarian origin. Males of many vertebrate classes, including fish, amphibians, and reptiles, have the ability to synthesize vitellogenin if stimulated by estrogen, although this does not occur normally. Intensive chemical fractionation of sewage identified two major classes of compounds capable of acting as estrogens in male fish; these included the pharmaceutical estrogen, ethinylestradiol, and the industrial chemicals, nonylphenol and octylphenol. Ethinylestradiol is a common ingredient of the human birth control pill and is excreted in the urine of females taking this pharmaceutical agent. Ethinylestradiol has been identified in the surface and reclaimed sewage waters from all continents where such studies have been performed. Similarly, non-ylphenol, an alkylphenolic chemical, is widely used in industrial applications as a surfactant and is commonly released into the environment. It is persistent in the ecosystem with very large concentrations found associated with sediments and organic matter in freshwater and estuarine regions. It has been shown to be weakly estrogenic in mammalian laboratory animals, but is a potent estrogen in many fish. Laboratory-based life-cycle testing with ecologically relevant concentrations has shown that both of these compounds have adverse effects on the reproductive potential ofmales and females, and they also alter sex determination in developing embryos. These common pollutants have the potential to disrupt the health of individual animals and the persistence of populations; some populations have no males. It has also been suggested that endocrine disruption could be associated with the decline of commercial and sport fish populations.
Alligators and Pesticides
Alligators and crocodiles are long-lived top predator species inhabiting most subtropical and tropical wetlands.
Studies begun in the late 1980s reported abnormalities in central and south Florida (USA) populations of the American alligator exposed to various contaminant mixtures associated with modern agriculture, such as insecticides, herbicides, and fertilizers. These abnormalities include altered plasma sex steroid profiles, gonadal, genital, and immune tissue anatomy, and hepatic steroid metabolism. Specifically, male alligators exposed in ovo (as embryos) to various pesticides, due to deposition in the eggs prior to being laid by the female, exhibit significantly reduced plasma testosterone concentrations, aberrant testicular morphology, and small penis size. Females from the same contaminated locations displayed significantly elevated plasma concentrations of estradiol as neonates but reduced concentrations as subadults. Subadult females also had elevated plasma concentrations of the potent androgen dihydrotestosterone. They also exhibit a high frequency of polyovular follicles, an ovarian abnormality associated with low fertility and high embryonic mortality. These contaminated populations have shown elevated embryonic mortality greater than 50%. Polyovular follicles are a documented outcome of exposure of women to the estrogenic drug diethylstilbes-trol during fetal life exposed as fetuses due to their mothers taking this drug during pregnancy, and these exposed women also suffer a decrease in fertility.
Populations displaying these abnormalities have elevated egg, tissue, or serum concentrations of a wide range of organochlorine pesticides or their metabolites, heavy metals, and other widely used agricultural chemicals, such as nitrates. Experimental exposure of developing alligator embryos to various organochlorine pesticides or their metabolites induces many of the abnormalities seen in wild populations, such as altered plasma hormone profiles and small penis size as well as altered sex determination. Concentrations required to induce these abnormalities were in the part per trillion to part per billion range, 100-1000 times lower in concentration than the reported levels in alligator eggs or serum.
Studies of mosquito fish from the same contaminated lakes indicate that the reported abnormalities are not limited to a single lake or species, as male mosquito fish have reduced tissue concentrations of testosterone, lower sperm counts, and altered reproductive behavior.
Many studies have documented the detrimental effects of pulp mill effluent on the environment over many decades. Classical ecotoxicology studies reported wide-scale disruption of populations, including the local extinction of many exposed freshwater or estuarine fish and invertebrate populations. Although modifications in the processing of pulp mill effluent have occurred over time, abnormalities persist. Studies from several
Canadian locations report altered hormone profiles in fish exposed to pulp mill effluent, including alterations in hypothalamic, gonadal, and adrenal hormones. Exposed fish displayed altered stress responses and altered reproductive performance.
Masculinization of females has also been reported. For example, female mosquito fish living below effluent outfalls from paper pulp mills develop a gonopodium, a modified anal fin found in males of this species and used to transfer sperm to the female for internal fertilization. The gonopodium develops in the male following exposure to androgens, specifically testosterone. Masculinized females do reproduce but have lower production of offspring and greatly elevated levels of aromatase activity in their brain and ovary. Aromatase is an enzyme that converts the hormone testosterone to estradiol, the principle estrogen in these females. These females thus have an altered potential to produce this critical hormone that regulates reproduction.
Fish, Feedlots, and Pharmaceuticals
Modern animal production techniques in many countries involve the use of potent hormones and antibiotics. Although there has been an ongoing debate on the safety of the meat products produced from such practices, few concerns have been voiced concerning the possible ecological impacts of these practices. Guillette and colleagues have examined feral fish exposed to effluent released from animal feedlots, including urine and feces, into a natural river system. They observed that male fish exhibited many of the classical signs of exogenous androgen exposure, including reduced testicular mass, reduced plasma testosterone, and altered head morphology. With the extensive use of anabolic steroids in cattle production, the potential for wide-scale disruption of fish reproduction is possible, since the presence of ethi-nylestradiol in rivers after excretion by women and bacterial action in water treatment plants leads to endocrine disruption in fish. Experimental laboratory-based studies support the field observations, as low-level exposure to the commonly used anabolic steroid trenbolone (used to promote growth in cattle) alters fish development and reproduction in a manner similar to that observed in the wild fish.
These and many more observations of wildlife demonstrate that global contamination of wildlife populations has dramatic effects on the health and reproductive potential of these populations. As described in Endocrine Disruptor Chemicals: Overview, the pheno-type observed in individuals is produced by the environment acting on the genotype. The abnormalities observed in wildlife are not due to classically held concepts of gene mutations. Instead, they represent alterations in the timing of gene expression and the level of gene expression. As described above, if exposure occurs during embryonic development, these alterations can be permanent.
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