Australasian Science Magazine

A large male Tasmanian devil with advanced facial tumours, the disease that has caused widespread and severe decline across the devil’s range.

By Tracey Hollings and Menna Jones

Brushtail possums are boldly venturing away from the safety of trees to forage on the ground as an unprecedented transmissible cancer removes their major predator, the Tasmanian devil.

Large predators are vanishing worldwide due to their vulnerability to habitat loss, emerging diseases and persecution. Predators protect biodiversity, and their loss has been attributed to changes in vegetation communities and the decline and even extinction of small wildlife.

Measuring the effects that big predators have on ecosystems is difficult because they live at large scales. “Natural experiments” – where environmental change occurs in the wild – offer an opportunity to observe large-scale ecosystem change and investigate the influence of large predators on ecosystems.

The unprecedented decline of the Tasmanian devil from a novel transmissible cancer is providing one such rare natural experiment. Spread by the transfer of live tumour cells when devils bite each other, Tasmanian devil facial tumour disease (DFTD) has spread from its origin in the north-east of Tasmania in the mid-1990s to most of the island state. Devil populations suffer immediate and dramatic local decline, to more than 90%, after 6 years. It’s expected that wild devil populations will remain suppressed for decades, although evolution of the devil and the tumour is expected to lead eventually to an endemic disease and devil recovery.

Apart from the 20th century extinction of the thylacine, Tasmania retains an almost intact community of mammals, and mammalian and avian carnivores. This is mainly because the island was spared the devastating consequences of introduced dingoes and foxes, which were responsible for the large number of mammal extinctions on mainland Australia.

Tasmania has also not suffered the extensive clearing of wildlife habitats observed elsewhere. However, the decline of Tasmania’s largest mammalian predator, the Tasmanian devil, is now triggering large-scale and potentially irreversible changes to this ecosystem.

The common brushtail possum is generally considered to be an arboreal browing herbivore, but possums will take calculated risks to descend to the ground to forage, where they are at risk of predation from terrestrial mammals. Brushtail possums are a common prey species of devils, and they are changing their behaviour in response to a reduced predation risk as devils disappear from the landscape.

In our study, published in Proceedings of the Royal Society B (www.tinyurl.com/hqvme8d), we assessed behavioural changes in brushtail possums using two different methods. The first involved non-invasive hair traps that use double-sided sticky tape to collect hair samples from animals that visit the baited traps. Sites with higher numbers of positive traps for a species indicate a higher activity of that species relative to sites with lower positive trap numbers. The second was “giving-up densities”, a method that uses artificial feeding stations to measure an individual’s perception of predation risk. Differences in the giving-up densities value, which is measured as the amount of food remaining in an artificial food patch at the end of the experimental period, reflect the differences in the risk of predation between the patches. The more food remaining, the higher the risk of predation and the less comfortable an animal is spending time foraging in the patch.

Prey must balance the need to forage with the risk of being eaten, and therefore finely tune their behaviours to maximise the first and minimise the latter. A reduced threat of predation can lead a species to relax, and in some cases lose, particular anti-predator behaviours because maintaining these costs energy.

Behavioural changes of prey are some of the most rapid responses to changing predator populations. Individuals may change their behaviour to take greater advantage of resources, such as foraging further from an area they perceive to be safe to take advantage of better quality food. This can have flow-on effects to reproductive success, with higher numbers of healthy offspring and therefore an increase in population abundance over time. In the case of brushtail possums, a predominantly arboreal herbivore, they may spend greater time on the ground and forage further from trees they can climb to evade terrestrial predators.

To test how the possums are recognising the lessening risk of predation as devil densities decline, we chose six sites in each of three regions across Tasmania defined by different lengths of time since the outbreak of DFTD. This time represents a proxy for devil population decline and subsequent predation pressure. The three regions were:

• the north-east of Tasmania, where the facial tumour disease originated 12–15 years prior to the study and where devil numbers are the lowest;
• the mid-north of Tasmania, where DFTD had been present for 4–7 years. This represents a declining devil population; and
• the north-west of Tasmania, where the facial tumour disease had not yet reached at the time of the study, so devil populations were at their naturally high density.

We also put out food patches on Maria Island, where at that time devils had never been present.

Each site comprised 10 food patches at least 100 metres apart. Food patches comprised a pair of specially designed feeding trays containing 100 sultanas mixed through river pebbles. One feeding tray was placed at the base of an “escape tree” that a possum could climb to evade a terrestrial predator, with the other feeding tray 5–12 metres from any escape tree in open ground. The distance to the nearest escape tree measured the potential “safety” or “riskiness” of the food tray.

To determine the species responsible for foraging in the food patch on a particular night, we used motion-activated cameras, or double-sided adhesive tape placed around the edge of the container and identified the hair collected. We chose sultanas as the food type because sultanas are highly tempting to brushtail possums and they retain their integrity when wet, so they could be easily identified and counted.

We deployed the food patches for a total of four nights. Each morning, if there was evidence of visitation, we counted the sultanas remaining and restored the food patch with 100 fresh sultanas. There was a lot of time spent counting more than 100,000 sultanas used in this experiment!

Our study provided compelling results for changing possum behaviour and activity patterns. Possums were present in all areas where devils are found, but the hair traps indicated that possum activity increased with the increasing number of years since the DFTD outbreak and subsequent population decline of devils. These changes in activity can be the result of behavioural changes or increased abundance – most likely a combination of both.

The “giving-up densities” results from the food patches tell us that possums are foraging further and for longer periods of time from trees that provide refuge from predators in areas where devil populations have been suppressed the longest. They also find the food patches faster in areas of low devil densities.

Possums in the north-west of Tasmania, which was disease-free at the time of the study and therefore still had high densities of healthy devils, were reluctant to forage away from the safety of trees. This method provides us with evidence for changes in behaviour irrespective of changing population density.

Within 15 years of the sustained decline in devils, possums have relaxed their behaviours to such an extent that they are now indistinguishable from possums on Maria Island, where devils had never been present. The few devils remaining in the landscape, when the disease has decimated the population by 90%, are therefore having a negligible effect on possum behaviour.

Possums are not losing all of their anti-predator behaviours though. They still maintain behaviours required to avoid other predators, including a preference for tree canopy cover that protects them from birds of prey.

Ecosystems are comprised of complex interactions between the different species and the abiotic environment. Behavioural changes in an ecosystem occur rapidly when the numbers of a key predator change, either through decline or introduction, and are a signal of broader changes occurring within the ecosystem.

Disruption to one key species can affect multiple species and trophic levels. For example, changes in the behaviour of a herbivore can lead to increased grazing pressure, which impacts vegetation communities. This can have further flow-on effects to other herbivores and invertebrates, and even lead to soil erosion.

We have not yet detected an increase in the abundance of possums, perhaps because possum numbers are driven strongly by rainfall and food availability. In agricultural and forestry areas, significant culling programs in place for grazing and crop protection also limit possum numbers.

Results from our other studies suggest that more changes are afoot in the Tasmanian ecosystem. Feral cats are increasing as devils decline, suggesting that high devil numbers formerly suppressed their activity and/or populations. Small native mammals, which are preyed upon by cats, are disappearing and being replaced by increasing numbers of invasive black rats. Black rats reproduce much faster and have better invasive predator recognition than native rodents, so they are better able to survive high densities of cats. Cats are the primary host for Toxoplasma gondii, a parasitic disease to which some native animals such as macropods and bandicoots are particularly susceptible. Toxoplasma is more prevalent in areas of long-term devil decline where there are more cats. Feral cats have been implicated in several Australian mammal extinctions on the mainland, and any increase could be a disaster for Tasmanian ecosystems.

The loss of large predators worldwide from large parts of their historic ranges is leading to the simplification of eco­systems. Complex and unexpected changes are cascading in ecosystems, affecting seemingly unrelated species. Some of these effects may be irreversible, such as when the loss of a top predator causes an increase in invasive middle-sized predators, which in turn causes the extinction of small mammals and birds.

Restoration of species such as large predators that have high influence in structuring ecosystems may be the key to stemming the flow of biodiversity loss.