Herbicide impacts marsupial reproduction and development

Marsupials are experiencing devastating population declines across Australia, with 21 per cent of native mammals currently threatened with extinction. Marsupials come under threat from habitat loss, climate change and predation from introduced species like foxes and cats.

Extreme weather events including those that preceded the bushfires of 2019-2020 are predicted to increase in both magnitude and frequency over the coming decades. All of these factors push our already vulnerable marsupial populations into more dire circumstances.

As their habitat becomes more restricted, marsupials are being further forced into agricultural areas, attracted to the food resources and rare permanent water sources. The shift to farmland increases their risk of exposure to agricultural contaminants, like pesticides.

Many pesticides are already well-known environmental toxins that can impact hormone signalling in our bodies. These so-called endocrine-disrupting chemicals (EDCs) have the ability to impact normal growth and development and cause disease.

One particular chemical of concern in Australia is the herbicide atrazine. Atrazine is used extensively on cereal crops and in forestation to prevent the growth of weeds.

Concentrations have been recorded at disturbingly high levels in Victorian rivers and Tasmanian streams immediately after forestry spraying.

Atrazine is so toxic that it has been banned across the European Union since 2003, due to its known impacts on the health of wildlife and potential impacts on humans.

Despite its ban in the EU, atrazine remains as one of the most widely used herbicides in Australia, with approximately 3000 tons used on crops annually.

Atrazine disrupts the signals from reproductive hormones during development and in adulthood. Exposures cause major abnormalities in the male reproductive system often causing male sterility or even male-to-female sex reversal in frogs.

Atrazine affects a broad range of animals from mammals like rats to amphibians, reptiles and even fish.

We examined whether atrazine was also capable of impacting the reproductive system of marsupials.

Marsupials have a unique mode of reproduction which may make them particularly sensitive to environmental toxins. They typically give birth to tiny young that complete their development external to their mother in her pouch.

The young are dependent on milk from their mother to develop. Many EDCs can accumulate in breast milk and are passed from mothers to their young after eating or drinking from contaminated resources.

The kangaroos and wallabies (Macropodid marsupials) are particularly at high risk because of their abundance in agricultural areas where they may graze on sprayed crops and drink from contaminated water resources where chemicals like atrazine accumulate from run off.

This is particularly a problem in Australia where we have limited rainfall, leading to often very high concentrations in precious water resources.

To mimic this route of exposure, we exposed five adult female tammar wallabies to atrazine contaminated water throughout pregnancy, birth and lactation. The study number was kept small for ethical reasons, to initially examine ‘poof of principle’ of the effects of atrazine.

The experimental concentration (450 ppm) are higher than the average levels in Australian waterways, but mimic potential exposure levels immediately after spraying.

Recorded concentrations of atrazine from monitoring across Australia can be viewed via this interactive map.

Macropodid marsupials would also graze on sprayed crops in addition to drinking from contaminated water sources, leading to potentially even higher levels of exposure than those examined here.

In our study the mothers were exposed until the pouch young were 200 days old, which is when they begin to leave the pouch and rely less on their mother’s milk. We then examined the reproductive development of their young by assessing the growth and development of the gonad and phallus.

The gonad forms the testis or ovary and the phallus becomes the penis or clitoris in males and females respectively. These organs are especially sensitive to the hormonal environment during development.

Although no structural abnormalities were seen in gonad structure, atrazine altered the expression of several genes required for normal testis function. Importantly, long-term exposure to atrazine resulted in a 20 per cent reduction in penis length in male young at the conclusion of the experiment.

These results demonstrate that atrazine exposure during gestation and lactation can significantly affect hormone signalling during development. This led to reduced penis length in male young, which would likely lead to altered reproductive success.

This is the first study to show that endocrine disruptors are able to affect developing marsupial pouch young through gestational and lactational exposure.

Given that atrazine has been banned in the EU because of its toxic impacts to wildlife, guidelines for its use in Australia should be reassessed and we would recommend that alternative herbicides are used, especially where marsupials are present.

Exposure to atrazine, and other EDCs, should be a consideration for marsupial conservation management.

Because of the overlapping distribution of macropodid marsupials with agricultural areas, these data raise major concerns for the use of pesticides in areas with vulnerable or endangered marsupial populations.

These findings illustrate the need for more stringent guidelines surrounding the use of known EDCs, such as atrazine, in Australia.

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