Ecological effects of disease-induced apex predator decline
Creators: name: Hollings, T
Publisher: name: University Of Tasmania
Year: 2023

description: The global extirpation of the world's apex predator fauna is consistently highlighting their important functional role in preserving biodiversity and maintaining ecosystem resilience. Apex predator declines and extinctions are promoting more invasive and homogenised ecosystem states, linked with secondary species extinctions, changes to community composition, and redefined carnivore guilds. In taxonomically and geographically diverse ecosystems devoid of apex predators similar general patterns expressed in community dynamics are emerging, such as mesopredator release, yet the magnitude and significance of the effects are driven by their context. The Tasmanian devil (Sarcophilus harrisii) is the largest extant marsupial carnivore and is facing the real threat of disease induced extinction in the wild from a consistently fatal transmissible cancer, devil facial tumour disease (DFTD). The devil is now effectively the apex mammalian predator in Tasmanian ecosystems following the extinction of the thylacine (Thylacinus cynocephalus) but DFTD is threatening its ecological role in the environment. Since the disease arose in the early to mid 1990s devil populations have suffered declines in excess of 95% in long-term disease areas, and it has infected more that 75% of their current geographic range. Tasmania retains the most intact guild of marsupial carnivores in Australia and maintains healthy populations of many native mammal and bird species that are extinct or threatened on mainland Australia. The loss of Tasmanian devils over large tracts of Tasmania is of tremendous conservation concern for native biodiversity and community resilience. This study provides the first assessment of the ecosystem effects of Tasmanian devil decline and aims to determine overarching effects of the loss of an ecologically functional devil population on terrestrial mammalian fauna. Within the scope of this thesis, broad concepts encompassing abundance, behaviour and disease ecology of native and introduced species are assessed within four discrete projects. I utilised complimentary approaches with the benefit of this unique large scale natural experiment to assess common theories as well as considering less widely examined concepts which may be pertinent to global apex predator demise. First, using a state-wide spotlighting database which pre-dates DFTD by more than a decade, I evaluated the mesopredator release hypothesis (MRH) and the extent to which mesopredators are regulated by top-down or bottom-up environmental processes. Second, I conducted a rapid snapshot survey across a large spatial extent encompassing different devil densities to assess changes to community composition, invasive system states and the cascading effects of mesopredator release on populations of their prey. Third, I measured risk-sensitive behaviour of the common brushtail possum, a species regularly preyed upon by Tasmanian devils, employing a 'giving up densities' approach across a DFTD arrival gradient, which represents a proxy for devil population decline over time. Finally, following the evidence for mesopredator release of feral cats, I assessed whether there was potential for increased disease transmission of Toxoplasma gondii, a parasite whose only known definitive hosts are members of the Felid family but that can infect all warm-blooded mammals. This study provided several lines of evidence for a shifting ecosystem state and increasing threats to the persistence of native biodiversity in response to declining devil populations. Less diverse communities and a strong tendency towards more invasive system states were characteristic of areas with long-term devil decline. Native and introduced mammals responded differently to devil decline, and the direction of the response for species of each origin was consistent across different trophic levels. I found strong evidence for mesopredator release of the invasive feral cat (Felis catus) in response to devil decline and a concomitant decline and changing activity times in the much smaller native eastern quoll (Dasyurus viverrinus), suggesting that they may be indirectly protected by devils. Despite the comparable size and prey range of native spotted-tailed quolls (Dasyurus maculatus) to feral cats, there was no evidence of a similar response, notwithstanding some evidence for different activity times across different devil densities. The magnitude of the responses of mesopredators to declining devil populations was significantly affected by environmental variables. In anthropogenically dominated landscapes bottom-up control appears to be the principal regulating force, and in less disturbed areas top-down control is stronger. There was evidence for an increasingly invasive state, represented by a significantly higher proportion of activity of feral cats and introduced small mammals, which appeared to be affecting native prey species. Small- and medium-sized native species within the prey size range of large mesopredators showed population declines analogous to the declines observed in devil populations and also evidence for increased predation pressure, indicating that apex predator loss in Tasmania is threatening native biodiversity. There was evidence of behavioural responses in prey species to the decline in devil numbers. Using the giving up densities approach, I found evidence that the predominantly arboreal brushtail possum (Trichosurus vulpecula), a common prey item of devils, has changed its anti-predator behaviours and has increased its ground foraging activity in response to declining devil populations, whilst maintaining vigilant behaviours appropriate for the avoidance of other predator species. Behavioural responses have the potential to initiate a trophic cascade if changes in behaviour translate into increased fitness and reproductive output. Some native species are at risk from higher feral cat densities not only from increasing predation pressure but also from potentially amplified transmission of the Toxoplasma parasite. Australian native marsupials may be particularly susceptible to acute Toxoplasma, a consequence likely attributable to a lack of co-evolution. I found tentative support for higher prevalence rates in areas with higher cat densities and also a strong link to increased susceptibility in native species at higher trophic levels. There was also some suggestion for reduced behavioural reactions in infected individuals, with the potential to increase predation rates. This was among the first research that has investigated changing disease dynamics in response to mesopredator release, and represents an important and novel step towards more wide-ranging research of the effects of apex predator loss on biodiversity. The combined results, derived from empirical approaches, provide compelling evidence that diverse and complex changes are occurring in Tasmania's fauna communities following apex predator decline. The evidence is indicative of extensive and far-reaching consequences in the Tasmanian ecosystem, threatening native biodiversity and promoting alternative ecosystem states. The lessons learned from applying existing community ecology theories and approaches to this unique large scale natural experiment are applicable to other ecosystems confronted with apex predator loss and highlight the importance of a multifaceted and comprehensive approach to apex predator studies.