Endangered Australian top predator is frequently exposed to anticoagulant rodenticides.

Anticoagulant rodenticides (ARs) used to control mammalian pest populations cause secondary exposure of predatory species throughout much of the world. It is important to understand the drivers of non-target AR exposure patterns as context for assessing long-term effects and developing effective mitigation for these toxicants. In Australia, however, little is known about exposure and effects of ARs on predators. We detected AR residues in 74% of 50 opportunistically collected carcasses of the Tasmanian wedge-tailed eagle (Aquila audax fleayi), an endangered apex predator. In 22% of birds tested, or 31% of those exposed, liver concentrations of second generation ARs (SGARs) were >0.1 mg/kg ww. Eagles were exposed to flocoumafen, a toxicant only available from agricultural suppliers, at an exceptionally high rate (40% of birds tested). Liver SGAR concentrations were positively associated with the proportion of agricultural habitat and human population density in the area around where each eagle died. The high exposure rate in a species not known to regularly prey upon synanthropic rodents supports the hypothesis that apex predators are vulnerable to SGARs. Our results indicate that AR exposure constitutes a previously unrecognized threat to Tasmanian wedge-tailed eagles and highlight the importance of efforts to address non-target AR exposure in Australia.

High Frequency of Lead Exposure in the Population of an Endangered Australian Top Predator, the Tasmanian Wedge-Tailed Eagle (Aquila audax fleayi).

Lead poisoning, mainly through incidental ingestion of lead ammunition in carcasses, is a threat to scavenging and predatory bird species worldwide. In Australia, shooting for animal control is widespread, and a range of native scavenging species are susceptible to lead exposure. However, the prevalence of lead exposure in Australia's scavenging and predatory birds is largely unknown. We evaluated the degree to which the Tasmanian wedge-tailed eagle (Aquila audax fleayi), an endangered Australian raptor and facultative scavenger, showed evidence of lead exposure. We detected lead in 100% of femur and liver tissues of 109 eagle carcasses opportunistically collected throughout Tasmania between 1996 and 2018. Concentrations were elevated in 10% of 106 liver (>6 mg/kg dry wt) and 4% of 108 femur (>10 mg/kg dry wt) samples. We also detected lead in 96% of blood samples taken from 24 live nestlings, with 8% at elevated concentrations (>10 µg/dL). Of the liver samples with elevated lead, 73% had lead207/206 isotope ratios within the published range of lead-based bullets available in Tasmania. These first comprehensive data on lead exposure of an Australian raptor are comparable to those for raptor studies elsewhere that identify lead-based ammunition exposure as a conservation threat. Our findings highlight the importance of further research and efforts to address lead contamination throughout the Tasmanian ecosystem and in other Australian regions. Environ Toxicol Chem 2021;40:219-230. © 2020 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC. This article has been contributed to by US Government employees and their work is in the public domain in the USA.

Disease-induced decline of an apex predator drives invasive dominated states and threatens biodiversity.

Apex predators are important in protecting biodiversity through top-down influence on food webs. Their loss is linked with competitive release of invasive mesopredators and species extinctions. The Tasmanian devil (Sarcophilus harrisii) has experienced severe declines over a 15-yr period as a novel transmissible cancer has spread across its current geographic range. We surveyed the mammalian community, using hair traps, across the spatial extent of the devil's progressive population decline. We found increased activity of alien invasive species (feral cats, black rats), and reduced small and medium-sized native prey species in response to the timing of the decline. In areas of long-term devil decline, invasive species comprised a significantly larger proportion of the community. The results provide evidence that the devil plays a keystone role in Tasmania's ecosystem with their decline linked to a shift toward an invasive state and biodiversity loss in one of Australia's most intact faunal communities.

Relaxation of risk-sensitive behaviour of prey following disease-induced decline of an apex predator, the Tasmanian devil.

Apex predators structure ecosystems through lethal and non-lethal interactions with prey, and their global decline is causing loss of ecological function. Behavioural changes of prey are some of the most rapid responses to predator decline and may act as an early indicator of cascading effects. The Tasmanian devil (Sarcophilus harrisii), an apex predator, is undergoing progressive and extensive population decline, of more than 90% in long-diseased areas, caused by a novel disease. Time since local disease outbreak correlates with devil population declines and thus predation risk. We used hair traps and giving-up densities (GUDs) in food patches to test whether a major prey species of devils, the arboreal common brushtail possum (Trichosurus vulpecula), is responsive to the changing risk of predation when they forage on the ground. Possums spend more time on the ground, discover food patches faster and forage more to a lower GUD with increasing years since disease outbreak and greater devil population decline. Loss of top-down effects of devils with respect to predation risk was evident at 90% devil population decline, with possum behaviour indistinguishable from a devil-free island. Alternative predators may help to maintain risk-sensitive anti-predator behaviours in possums while devil populations remain low.

Trophic cascades following the disease-induced decline of an apex predator, the Tasmanian devil.

As apex predators disappear worldwide, there is escalating evidence of their importance in maintaining the integrity and diversity of the ecosystems they inhabit. The largest extant marsupial carnivore, the Tasmanian devil (Sarcophilus harrisii) is threatened with extinction from a transmissible cancer, devil facial tumor disease (DFTD). The disease, first observed in 1996, has led to apparent population declines in excess of 95% in some areas and has spread to more than 80% of their range. We analyzed a long-term Tasmania-wide data set derived from wildlife spotlighting surveys to assess the effects of DFTD-induced devil decline on populations of other mammals and to examine the relative strength of top-down and bottom-up control of mesopredators between 2 regions with different environmental conditions. Collection of the data began >10 years before DFTD was first observed. A decrease in devil populations was immediate across diseased regions following DFTD arrival, and there has been no indication of population recovery. Feral cats (Felis catus) increased in areas where the disease was present the longest, and feral cat occurrence was significantly and negatively associated with devils. The smallest mesopredator, the eastern quoll (Dasyurus viverrinus), declined rapidly following DFTD arrival. This result suggests the species was indirectly protected by devils through the suppression of larger predators. Rainfall deficiency was also a significant predictor of their decline. Environmental variables determined the relative importance of top-down control in the population regulation of mesopredators. In landscapes of low rainfall and relatively higher proportions of agriculture and human settlement, top-down forces were dampened and bottom-up forces had the most effect on mesopredators. For herbivore prey species, there was evidence of population differences after DFTD arrival, but undetected environmental factors had greater effects. The unique opportunity to assess population changes over extensive temporal and spatial scales following apex predator loss further demonstrated their role in structuring ecosystems and of productivity in determining the strength of top-down control.

Wildlife disease ecology in changing landscapes: Mesopredator release and toxoplasmosis.

Changing ecosystem dynamics are increasing the threat of disease epidemics arising in wildlife populations. Several recent disease outbreaks have highlighted the critical need for understanding pathogen dynamics, including the role host densities play in disease transmission. In Australia, introduced feral cats are of immense concern because of the risk they pose to native wildlife through predation and competition. They are also the only known definitive host of the coccidian parasite, Toxoplasma gondii, the population-level impacts of which are unknown in any species. Australia's native wildlife have not evolved in the presence of cats or their parasites, and feral cats may be linked with several native mammal declines and extinctions. In Tasmania there is emerging evidence that feral cat populations are increasing following wide-ranging and extensive declines in the apex predator, the Tasmanian devil, from a consistently fatal transmissible cancer. We assess whether feral cat density is associated with the seroprevalence of T. gondii in native wildlife to determine whether an increasing population of feral cats may correspond to an increased level of risk to naive native intermediate hosts. We found evidence that seroprevalence of T. gondii in Tasmanian pademelons was lower in the north-west of Tasmania than in the north-east and central regions where cat density was higher. Also, samples obtained from road-killed animals had significantly higher seroprevalence of T. gondii than those from culled individuals, suggesting there may be behavioural differences associated with infection. In addition, seroprevalence in different trophic levels was assessed to determine whether position in the food-web influences exposure risk. Higher order carnivores had significantly higher seroprevalence than medium-sized browser species. The highest seroprevalence observed in an intermediate host was 71% in spotted-tailed quolls (Dasyurus maculatus), the largest mammalian mesopredator, in areas of low cat density. Mesopredator release of cats may be a significant issue for native species conservation, potentially affecting the population viability of many endangered species.

Mitochondrial DNA offers unique insights into invasion history of the common starling.

Mitochondrial DNA (mtDNA) can be a powerful genetic marker for tracing origins and history of invasive populations. Here, we use mtDNA to address questions relevant to the understanding of invasion pathways of common starlings (Sturnus vulgaris) into Western Australia (WA) and discuss the utility of this marker to provide information useful to invasive species management. Mitochondrial sequence data indicate two geographically restricted genetic groups within Australia. Evidence of dispersal from genetically distinct sources outside the sampled range of starlings in Australia suggests increased vigilance by management agencies may be required to prevent further incursions from widely separated localities. Overall, genetic diversity in Australia was lower than in samples from the native range. Within Australia, genetic diversity was lowest in the most recently colonized area in the west, indicating that demographic bottlenecks have occurred in this area. Evidence of restricted dispersal between localities on the edge of the range expansion (ERE) in WA and other Australian sampling localities suggests that localized control within the ERE may be effective in preventing further range expansion. Signatures of spatial and demographic expansion are present in mismatch analyses from sampling localities located at the ERE, but neutrality indices did not support this finding, suggesting that the former may be more sensitive to recent expansion. Additionally, mismatch analyses support the presence of admixture, which is likely to have occurred pre-introduction. We compare our findings with those from a microsatellite study of the same samples and discuss how the mtDNA analyses used here offer valuable and unique insights into the invasion history of introduced species.