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Reproductive Threats to Australia’s Marsupials

davemhuntphoto/Adobe

Credit: davemhuntphoto/Adobe

By Andrew Pask

Chemicals used in agriculture, industry and household goods can have effects on marsupial fertility as profound as sex reversal.

Synthetic and naturally occurring chemicals released into the environment can have disastrous effects on reproduction, and are becoming a matter of global concern. These environmental endocrine disruptors (EEDs) have major impacts on sexual development in humans as well as populations of wild animals.

EEDs have been identified in many everyday items, including plastic bottles and food containers, canned foods, fresh foods, detergents, toys, cosmetics and pesticides. Some EED compounds naturally occur in introduced plant species such as soya and subterranean clover. Many of these compounds are commonly used in agriculture, suburban environments and in the home.

EED levels in the Australian environment are on the rise, and in many instances exceed levels known to have devastating effects on animal populations in the USA and Europe. EED levels are especially high in areas surrounding intensive livestock operations, in waterways surrounding wastewater treatment plants, paper mills and in agricultural areas.

With reduced rainfall and extended drought conditions becoming a regular event over much of Australia, these toxic chemicals can become highly concentrated in catchments, posing a significant risk to many native species dependent on such resources.

It is now widely accepted that many diseases and developmental disorders observed in mammals are the result of exposure to environmental toxicants during early development in the womb. EEDs can interfere with the normal hormonal cues required in the developing embryo, and can profoundly affect the development of the reproductive system. Not surprisingly, EEDs are having a major impact on wildlife.

The effect of EEDs on aquatic species has been studied extensively, but their effects are much less well understood in terrestrial animals. Furthermore, there are almost no studies that have examined the impact of these chemicals on Australia’s marsupials.

Australian marsupials are exposed to a wide range of EEDs from agricultural and industrial contaminants as well as natural toxins in their diet. Research has shown that marsupials are especially sensitive to alterations to their hormonal environment during development. These hormonal alterations can have a profound effect on sex determination, causing sex reversal in some cases and reduced fertility. Thus it appears that EED exposure is of major concern to marsupial health.

Furthermore, many of Australia’s marsupial species are experiencing population decline. While habitat loss and species introduction is undoubtedly a major contributor to this decline, exposure to foreign chemicals, such as EEDs, has the potential to have a major impact on marsupial species in certain environments.

Marsupials have many unique features of their development and physiology that affect their ability to tolerate EED exposures and consequently make them more susceptible to their negative effects than eutherian/placental mammals. Marsupials are born in a highly under-developed state. Most marsupial growth and development occurs after birth, in the pouch, while the young is dependent on milk. If the mother’s nutritional intake becomes contaminated with EEDs, the young will be compromised because they have no ability to remove or detoxify these chemicals due to the immaturity of their organs.

Even before birth, marsupials have only a very short-lived placenta, providing little potential for detoxifying EEDs absorbed from the mother’s circulation. This is in contrast to most eutherian mammals, including humans, that develop a complex and long-lived placenta that is able to break down many hormones and their metabolites.

Eutherian mammals also undergo differentiation of their organ systems before birth, while they remain coupled to the mother’s detoxification systems, providing some additional protection from EED exposures. In humans, many EEDs accumulate in fatty tissues and can be passed through the milk during lactation. Consequently, the extended period of lactation in marsupials while the young develop in the pouch could cause an increased and prolonged exposure to EEDs.

Of greater concern is the fact that the marsupial urogenital tract and gonads do not differentiate until around the time of birth and are especially susceptible to endocrine disruption at this time.

Some of the most destructive EEDs are those that mimic the naturally occurring oestrogen hormone. Oestrogen is typically thought of as a female hormone, but is actually essential for reproductive health and fertility in both males and females and is tightly regulated during our developing and adult lives.

Oestrogen-mimicking chemicals are at an all time high in Australian waterways. The majority of these contaminants come in the form of oestrone and oestradiol, which remain as active compounds in run-off from agriculture and wastewater-treatment plants. Terrestrial animals that rely on these water sources will be exposed to these active oestrogen compounds.

The pesticide endosulphan, which has potent oestrogen-mimicking properties, was only banned in Australia in 2010. Before its ban, 260 tonnes per year were sprayed on Australian crops.

In addition, oestrogenic EEDs can be found from natural origins. Subterranean clover (Trifolium subterraneum), which is seeded as animal fodder in areas with poor quality soil, covers literally millions of hectares across every state in Australia. The clover produces high levels of a chemical called genistein and lower quantities of daidzein, both of which are potent oestrogen-like compounds that cause many reproductive defects in sheep and mice when ingested in large quantities. Grazing marsupial species could potentially consume these plant,s leading to oestrogen exposure to their gestating young or young in the pouch.

Oestrogen compounds can drastically affect sexual development in marsupials. High levels of oestrogen can cause complete male-to-female sex reversal, while lower levels cause abnormalities to testis development and infertility. Even slight alterations to the development of the early testis or ovary can have profound effects on the masculinisation or feminisation of the resulting young, further leading to reduced fertility and lower fitness. Thus, oestrogenic EEDs are likely to pose a significant risk to marsupial populations in the environment.

In addition to oestrogen-like EEDs, some environmental pollutants have anti-androgenic properties, and again these pose a potential health risk to our native fauna. Androgens are typically thought of as male hormones but they have important roles in both sexes.

Testosterone is an androgen, and a reduction in its activity can cause many reproductive defects, including reduced fertility and hypospadias. Hypospadias is a condition caused by a failure of urethral closure during penis development, and is one of the most common human birth defects in Australia, currently affecting approximately one in every 125 live male births. Anti-androgenic exposure in developing marsupials also causes mild to severe forms of hypospadias. In the wild, severe hypospadias would lead to infertility and increased risk of infections.

The potent anti-androgen atrazine is one of the most widely used herbicides in Australian agriculture, with over 116 tonnes released into the environment each year. Atrazine causes major reproductive abnormalities in vertebrates, from frogs to rats and humans. This chemical is a widely used herbicide for the control of weeds in maize, sorghum, sugarcane, timber plantations, lucerne, grass seed crops and potatoes. Atrazine is also used for weed control prior to planting and for fallow maintenance. All such agricultural areas are home to many marsupial species, which graze in high numbers on the treated crops and drink from irrigation channels and dams surrounding these areas.

In addition to atrazine, diazinon and dichlorvos are another two pesticides currently used in Australia with known anti-androgenic effects. Many others exist.

Thus, our native fauna are currently developing in an environment surrounded by endocrine-disrupting chemicals but we don’t have a full understanding of their potential impacts on species fitness and survival.

One of the biggest concerns is the potential long-term effects that EED exposures can have on fertility. Studies in humans and mice exposed to large amounts of endocrine disruptors during development have shown that the individuals have decreased fertility and reproductive abnormalities as well as an increased risk of developing reproductive cancers.

In addition, the offspring of individuals who were exposed to EEDs also experience greatly increased rates of reproductive abnormalities and reproductive cancers. Many groups are now examining the potential for endocrine disruptors to alter our DNA’s epigenetic code in ways that might cause defects to persist for multiple generations.

Thus there is a critical need to determine how severe the impacts of different EEDs might be in different marsupial species. Such research is absolutely critical to defining the potential impacts of EED chemicals on the sustainability of our native mammals and in the development of management policies for the use of such chemicals in our environment.

Andrew Pask is an ARC Future Fellow and Associate Professor and Reader in the School of BioSciences at The University of Melbourne.