Clare E. Hawkins

Distribution and Impacts of Tasmanian Devil Facial Tumor Disease

The Tasmanian devil, Sarcophilus harrisii, is the largest extant marsupial carnivore. In 1996, a debilitating facial tumor was reported. It is now clear that this is an invariably lethal infectious cancer. The disease has now spread across the majority of the range of the species and is likely to occur across the entire range within 5 to 10 years. The disease has lead to continuing declines of up to 90% and virtual disappearance of older age classes. Mark-recapture analysis and a preliminary epidemiological model developed for the population with the best longitudinal data both project local extinction in that area over a timeframe of 10 to 15 years from disease emergence. However, the prediction of extinction from the model is sensitive to the estimate of the latent period, which is poorly known. As transmission appears to occur by biting, much of which happens during sexual encounters, the dynamics of the disease may be typical of sexually transmitted diseases. This means that transmission is likely to be frequency-dependent with no threshold density for disease maintenance. Extinction over the entire current range of the devil is therefore a real possibility and an unacceptable risk.

Life-history change in disease-ravaged Tasmanian devil populations

Changes in life history are expected when new sources of extrinsic mortality impact on natural populations. We report a new disease, devil facial tumor disease, causing an abrupt transition from iteroparity toward single breeding in the largest extant carnivorous marsupial, the Tasmanian devil (Sarcophilus harrisii), in which males can weigh as much as 14 kg and females 9 kg. This change in life history is associated with almost complete mortality of individuals from this infectious cancer past their first year of adult life. Devils have shown their capacity to respond to this disease-induced increased adult mortality with a 16-fold increase in the proportion of individuals exhibiting precocious sexual maturity. These patterns are documented in five populations where there are data from before and after disease arrival and subsequent population impacts. To our knowledge, this is the first known case of infectious disease leading to increased early reproduction in a mammal. The persistence of both this disease and the associated life-history changes pose questions about longer-term evolutionary responses and conservation prospects for this iconic species.

Food Habits of an Endangered Carnivore, Cryptoprocta ferox, in the Dry Deciduous Forests of Western Madagascar

Abstract We describe the diet of fossas (Cryptoprocta ferox) in a dry deciduous forest of western Madagascar from 376 scats collected between June 1994 and September 1996, from which 554 prey items were identified. More than 90% of these were vertebrates, and more than 50% were lemurs. No other nonprimate mammal includes such a high proportion of primate items in its diet. The principal prey comprised approximately 6 lemur species and 2 or 3 spiny tenrec species, along with snakes and small mammals. Significant differences were apparent in the composition of the scats in wet and dry seasons, with a higher proportion of Tenrec in the former, and fewer lemurs. Within the confines of a diet of vertebrates, fossas appeared to be opportunistic predators. For those prey types for which data were available, a significant relationship was found between the estimated relative number of individuals taken of any one type of prey and its abundance. Fossas were estimated to remove up to 19% of their prey populations per year. This high impact suggests that they were living close to the maximum population density possible on the available prey. Species of a wide range of body masses were included in the diet. Verreauxs sifaka (Propithecus verreauxi), weighing more than one-half of the body mass of the fossa, constituted approximately 11% of the prey biomass.

Transient Masculinization in the Fossa, Cryptoprocta ferox (Carnivora, Viverridae)

Abstract In at least 9 mammalian species, females are masculinized throughout life, but the benefits of this remain unclear despite decades of thorough study, in particular of the spotted hyaena (Crocuta crocuta) in which the phenomenon has been associated with a high fitness cost. Through examination of wild and captive fossas (Cryptoprocta ferox, Viverridae), androgen assays, and DNA typing for confirmation of gender, we made the first discovery of transient masculinization of a female mammal. Juvenile female fossas exhibited an enlarged, spinescent clitoris supported by an os clitoridis and a pigmented secretion on the underpart fur that in adults was confined to males. These features appeared to diminish with age. The majority of adult females lacked them, and os clitoridis length was inversely related to head-body length. No evidence was found to link this masculinization to elevated female androgen levels. Circulating concentrations of testosterone and androstenedione, but not dihydrotestosterone, were significantly lower in females than in males. No significant differences in testosterone, androstenedione, or dihydrotestosterone levels were found between juvenile (masculinized) and adult (nonmasculinized) females. There are several possible physiological mechanisms for this masculinization. None of the hypotheses so far proposed to explain the evolutionary basis of female masculinization in mammals are applicable to our findings. We present 2 new hypotheses for testing and development.

Devil Declines and Catastrophic Cascades: Is Mesopredator Release of Feral Cats Inhibiting Recovery of the Eastern Quoll?

The eastern quoll (Dasyurus viverrinus) is a medium-sized Australian marsupial carnivore that has recently undergone a rapid and severe population decline over the 10 years to 2009, with no sign of recovery. This decline has been linked to a period of unfavourable weather, but subsequent improved weather conditions have not been matched by quoll recovery. A recent study suggested another mechanism: that declines in Tasmanian devil (Sarcophilus harrisii) populations, due to the spread of the fatal Devil Facial Tumour Disease, have released feral cats (Felis catus) from competitive suppression, with eastern quoll declines linked to a subsequent increase in cat sightings. Yet current evidence of intraguild suppression among devils, cats and quolls is scant and equivocal. We therefore assessed the influences of top-down effects on abundance and activity patterns among devils, feral cats and eastern quolls. Between 2011 and 2013, we monitored four carnivore populations using longitudinal trapping and camera surveys, and performed camera surveys at 12 additional sites throughout the eastern quoll’s range. We did not find evidence of a negative relationship between devil and cat abundance, nor of higher cat abundance in areas where devil populations had declined the longest. Cats did not appear to avoid devils spatially; however, there was evidence of temporal separation of cat and devil activity, with reduced separation and increasing nocturnal activity observed in areas where devils had declined the longest. Cats and quolls used the same areas, and there was no evidence that cat and quoll abundances were negatively related. Temporal overlap in observed cat and quoll activity was higher in summer than in winter, but this seasonal difference was unrelated to devil declines. We suggest that cats did not cause the recent quoll decline, but that predation of juvenile quolls by cats could be inhibiting low density quoll populations from recovering their former abundance through a ‘predator pit’ effect following weather-induced decline. Predation intensity could increase further should cats become increasingly nocturnal in response to devil declines.

Evidence of rapid population decline of the eastern quoll (Dasyurus viverrinus) in Tasmania

Australia’s mammalian fauna has suffered unparalleled extinctions and declines in recent history. Tasmania has remained largely unaffected by these losses; however, marsupial dynamics are changing rapidly and new threats are emerging. Once abundant throughout south-eastern Australia, the eastern quoll (Dasyurus viverrinus) survives only in Tasmania. Until recently, it was considered widespread and common, but it may be undergoing a rapid and severe decline. The aim of this study was to quantify changes in eastern quoll populations over recent years. Data were compiled from statewide spotlight surveys, repeated historic trapping surveys and bycatch records from non-target trapping surveys. Spotlight surveys from 150 sites across Tasmania revealed a 52% reduction in the number of eastern quoll sightings over the 10 years to 2009. Declines of 61–100% were observed in trapping surveys at three study sites compared with trapping conducted 18–31 years earlier. A reduction in trap success was recorded in five of six non-target surveys, with declines of 51–100% over 1–12 years. These results suggest that the eastern quoll can no longer be presumed secure in Tasmania. Urgent management action may be needed to ensure the future conservation of the species in its last remaining stronghold.

Testing the Role of Climate Change in Species Decline: Is the Eastern Quoll a Victim of a Change in the Weather?

To conserve a declining species we first need to diagnose the causes of decline. This is one of the most challenging tasks faced by conservation practitioners. In this study, we used temporally explicit species distribution models (SDMs) to test whether shifting weather can explain the recent decline of a marsupial carnivore, the eastern quoll (Dasyurus viverrinus). We developed an SDM using weather variables matched to occurrence records of the eastern quoll over the last 60 years, and used the model to reconstruct variation through time in the distribution of climatically suitable range for the species. The weather model produced a meaningful prediction of the known distribution of the species. Abundance of quolls, indexed by transect counts, was positively related to the modelled area of suitable habitat between 1990 and 2004. In particular, a sharp decline in abundance from 2001 to 2003 coincided with a sustained period of unsuitable weather over much of the species’ distribution. Since 2004, abundance has not recovered despite a return to suitable weather conditions, and abundance and area of suitable habitat have been uncorrelated. We suggest that fluctuations in weather account for the species’ recent decline, but other unrelated factors have suppressed recovery.

Action needed to prevent extinctions caused by disease.

Your News in Brief item ‘Cancer forces Tasmanian devil onto endangered list’ highlights the plight of this carnivorous marsupial (Sarcophilus harrisii), driven towards extinction by devil facial-tumour disease, which is contagious

Density trends and demographic signals uncover the long‐term impact of transmissible cancer in Tasmanian devils

1. Monitoring the response of wild mammal populations to threatening processes is fundamental to effective conservation management. This is especially true for infectious diseases, which may have dynamic and therefore unpredictable interactions with their host. 2. We investigate the long-term impact of a transmissible cancer, devil facial tumour disease (DFTD), on the endemic Tasmanian devil. We analyse trends in devil spot-light counts and density across the area impacted by the disease. We investigate the demographic parameters which might be driving these trends, and use spatial capture-recapture models to examine whether DFTD has affected home range size. 3. We found that devils have declined by an average of 77% in areas affected by DFTD, and that there is a congruent trend of ongoing small decline in spotlight counts and density estimates. Despite this, devils have persisted to date within each of nine monitoring sites. One site is showing as yet unexplained small increases in density 8-10 years after the emergence of DFTD. 4. We also found the prevalence of DFTD has not abated despite large declines in density and that diseased sites continue to be dominated by young devils. The long-term impact of the disease has been partially offset by increased fecundity in the form of precocial breeding in 1-year-old females, and more pouch young per female in diseased sites. The lower densities resulting from DFTD did not affect home range size. 5. Synthesis and applications. Transmission of devil facial tumour disease continues despite large declines in devil density over multiple generations. Plasticity in life history traits has ameliorated the impact of devil facial tumour disease, however broad-scale trends in density show ongoing decline. In light of this, devil facial tumour disease and the impact of stochastic events on the reduced densities wrought by the disease, continue to threaten devils. In the absence of methods to manage disease in wild populations, we advocate managing the low population densities resulting from disease rather than disease per se.