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EcoHealth ( 2007) DOI: 10.1007/s10393-007-0120-6 2007 EcoHealth Journal Consortium Special Focus: Tasmanian Devil Declines Conservation Management of Tasmanian Devils in the Context of an Emerging, Extinction-threatening Disease: Devil Facial Tumor Disease Menna E. Jones,1,2 Peter J. Jarman,3 Caroline M. Lees,4 Heather Hesterman,1,2 Rodrigo K. Hamede,1 Nick J. Mooney,2 Dydee Mann,2 Chrissy E. Pukk,2 Jemma Bergfeld,5 and Hamish McCallum1 1 School of Zoology, University of Tasmania, Private Bag 5, Hobart, Tasmania, Australia Wildlife Management Branch, Department of Primary Industries and Water, Hobart, Tasmania, Australia 3 School of Ecosystem Management, University of New England, Armidale, New South Wales, Australia 4 Australasian Regional Association of Zoological Parks and Aquaria, Mosman, PO Box 20, New South Wales, Australia 5 Diagnostic Services, Department of Primary Industries and Water, King’s Meadows, Tasmania, Australia 2 Abstract: An emerging infectious facial cancer threatens Tasmanian devils with extinction. The disease is likely to occur across the range of the devil within 5 years. This urgent time frame requires management options that can be implemented immediately: the establishment of insurance populations, in captivity, wild-living on islands, and aiming for eradication in areas that can be isolated. The long-term options of the spontaneous or assisted evolution of resistance or development of a field-deliverable vaccine are unlikely to be available in time. The disease’s characteristic allograft transmission through intimate contact simplifies isolation of insurance populations and breaking transmission in suppression trials. Better knowledge of contact matrices in wild devils will help focus timing and demographic targets of removals. A metapopulation approach is needed that integrates captive and wild-living island and peninsula (disease suppression) populations to minimize the loss of genetic diversity over 50 years until either extinction and reintroduction can occur, resistance evolves or a fielddeliverable vaccine is developed. Given the importance of the insurance populations and the low genetic diversity of devils, a conservative target for retention of 95% genetic diversity is recommended. Encouraging preliminary results of the first disease-suppression trial on a large peninsula show fewer late stage tumors and no apparent population decline. Limiting geographic spread or suppressing the disease on a broadscale are both unlikely to be feasible. Since the synergy of devil decline and impending fox establishment could have devastating consequences for Tasmanian wildlife, it is crucial to manage the dynamics of new and old predator species together. Keywords: emerging wildlife disease, disease management, Tasmanian devil facial tumor disease, extinction risk, carnivorous marsupial, ecosystem impacts INTRODUCTION Correspondence to: Menna E. Jones, e-mail: [email protected] The facial tumor epidemic afflicting the wild population of Tasmanian devils, Sarcophilus harrisi, presents a real and unacceptable risk of extinction. The known rate of disease Menna E. Jones et al. spread (McCallum et al., 2007) indicates that, without management interventions, it is highly likely that no disease-free populations of devils will exist in 5 years time. Moreover, there is a real possibility that all affected populations will die out within 15 years after disease arrival, given the observed rate of decline in affected populations (McCallum et al., 2007), and the likelihood that transmission is frequency, rather than density, dependent (Hamede et al., 2008). This article lays out an overall strategy for achieving the conservation aim ‘‘to maintain the Tasmanian devil as an ecologically functional species in the wild’’ (AUSVET, 2005) in the context of this emerging disease and likely future scenarios. We also consider how to manage the ecosystem-wide implications of devil decline. The serious and urgent conservation situation of the Tasmanian devil requires immediate management and research that will rapidly achieve conservation outcomes. This restricts management options to those that can be implemented immediately with current levels of knowledge (McCallum and Jones, 2006). What is needed are ‘‘insurance’’ populations protected from the disease that would maintain genetic and phenotypic diversity of the species until one of three events occurred: 1) the evolution of resistance, either spontaneously or through selective breeding; 2) the development of a field-deliverable vaccine (Woods et al., 2007; or 3) extinction in the wild throughout the Tasmanian mainland, in which case the disease itself would become extinct and reintroduction from the insurance population would be possible. These three events have the potential to turn the disease epidemic around and allow reestablishment of devils in the landscape as an ecologically functional species. While the long-term options of genetic selection for resistance or a field-deliverable vaccine (Woods et al., 2007) are worth exploring, success of either is uncertain and neither would be available sufficiently rapidly to provide confidence of mitigation of the risk of extinction in the wild. Although extinction in the wild in a time frame of about 20 years is a real possibility, it remains possible that the ‘‘steady state’’ outcome of the DFTD epidemic will be a mosaic of local extinctions and infected populations persisting at low density (Table 1). Whatever the eventual outcome, it is clear that insurance populations need to be able to maintain genetic diversity for about 50 years to enable reestablishment of reintroduced wild populations to take place. To eliminate an emerging disease requires reducing the reproductive rate of the disease R0 (equivalent to the number of secondary cases per primary case when the disease is rare) to below one, and any reduction in R0 will slow the rate of spatial spread. R0 can be reduced by limiting the time that infected individuals can transmit the disease or by reducing the rate of disease transmission per unit time (McCallum and Jones, 2006). Realistic options for reducing transmission are limited to establishing populations isolated from the disease and to implementing disease suppression, via removal of infected individuals, in isolatable areas already infected with the disease with the aim of disease eradication. Neither requires knowledge of the etiological agent; knowledge of direct transmission (Pearse and Swift, 2006) is justification enough to proceed with them. Many serious emerging diseases of livestock or humans must initially be managed on a large scale despite poor knowledge of the etiological agent (e.g., BSE). All field management of a new disease is initially untested; but a well-designed adaptive-management approach allows us to refine methods as we learn about the disease. Due to the nature of the tumor (i.e., it is poorly differentiated and highly neoplastic) and the fact that it will metastasize readily by hematogenous spread, this is not a tumor that is amenable to curative treatment by surgical excision [Stephen Pyecroft, personal communication]. A combination of surgical intervention and chemotherapy using cytotoxic drugs may be useful to extend the life of valuable genetic lineages in a captive situation but is not a practical option for wild-living populations. Similarly urgent is the need to investigate and mitigate the expected and potentially serious ecosystem changes resulting from the loss of the top predator from Tasmanian ecosystems (McCallum and Jones, 2006). The ecosystem consequences of devil decline could be more serious than the loss of this one species (McCallum and Jones, 2006). TRANSMISSION AND MANAGEMENT Practical management options reflect our knowledge that the disease is an infectious cell line (Pyecroft et al., 2007) transmitted by allograft (Pearse and Swift, 2006) and highly unlikely to grow in any other species (so alternative reservoir hosts do not exist; McCallum and Jones, 2006). Aerosol transmission is similarly unlikely, easing biosecurity concerns. Biting is the most likely route of transfer of tumor cells, and vertical transmission from mother to young appears unlikely (Pyecroft et al., 2007). Possible transmission via fomites such as infected carcasses cannot be discounted. In particular, transmission through Local extinctions and local disease-free populations Combinations of extinction, disease-free persistence and disease Local extinctions and local persistence with disease Wild populations persist on islands only Only captive populations persist — Extinction 3 4 7 8 6 As in 2 above, but with some local stochastic extinction — — Unacceptable risk Maintenance of captive colonies Possibly most likely outcome Actions for 2 and 3 above without intervention No current populations on Translocation to most islands islands, continuing bio-security maintenance Devils persist, but with disease, across most of their existing range 2 5 Removal of diseased Unlikely, given 10+ animals or ‘‘stamping out,’’ years of disease reintroduction after extinction persistence at Mt. William Vaccination, continued Sufficient early reproduction or other Possible, but current removal of diseased compensation, evolution of host or disease populations appear animals, treatment, still to be declining genetic management Sufficiently low movement between Unlikely, given current rates Increased barriers to populations of spread movement and removal of diseased individuals Sufficiently low movement between Possible Actions for 2 and 3 above populations Disease ‘‘burns out’’ Disease-free devils across their existing range Management action to increase likelihood 1 Likelihood without management Preconditions without management No. Outcome Table 1. Possible Outcomes of the DFTD Epidemic, Ranked in Order of Decreasing Conservation Desirability Achievable. risk of animals with latent disease being translocated, or subsequent introduction of disease Achievable Avoidable with appropriate management As above Unlikely on mainland Tasmania. Possible on islands or peninsulas Possible, but tools not yet available Low, but reintroduction feasible if wild extinction occurs Possible, but tools not yet available Likelihood of management increasing chance of this outcome Managing Tasmanian Devil Facial Tumor Disease Menna E. Jones et al. devils should occur just prior to the mating season and should target those age-and-sex classes showing the highest contact rates. They indicate that DFTD might behave like a frequency-dependent disease as is typical of sexually transmitted diseases. Therefore, although the contact rate during foraging at carcasses increases with population density, this may be overridden by frequency-dependent contact in courtship and mating. Management of contact rates through managed removal of carcasses is unlikely to affect transmission rates. A wild population cannot be sustained without mating which is when transmission is most likely; so management must focus on minimizing courtship and mating involving any diseased devils. Figure 1. Average number of mating partners of devils of different sex (males black, females gray) and age (year) classes at Narawntapu National Park, Tasmania, recorded using proximity loggers. A mate was defined as an adult male and female that spent a minimum of 8 hours together at a distance closer than 30 cm. cannibalism of dead diseased devils would have profound implications for disease dynamics (Anderson and May, 1981; Boots, 1998; Rudolf and Antonovics, 2007). Essentially, the need for direct and intimate contact between devils for transmission to occur simplifies the isolation of insurance populations and the breaking of transmission in suppression trials. Nevertheless, focused management needs to reflect the rates and networks of contacts between individuals of different ages and sexes, and the behavioral, reproductive, and life-history events that influence the contact matrix and the temporal dynamics of disease transmission (Loehle, 1995; Dobson and Foufopoulos, 2001; Cross et al., 2004; Woodroffe et al., 2006; Vicente et al., 2007). In most emerging diseases, the majority of transmission comes from a small number of ‘‘superspreader’’ individuals in the population (Lloyd-Smith et al., 2005; Meyers et al., 2005). Such knowledge can focus management on times of year or population classes or individuals to maximize disease suppression. Above a low background rate of injuries probably from interactions at carcasses, most injuries to devils appear to occur during the synchronized 6-week mating season (February–March) and affect adult males and adult females equally (Hamede et al., 2008). Preliminary data from proximity loggers on adult devils (Rodrigo Hamede, unpublished) show that age and sex affect contact rates of adults (Fig. 1). These findings suggest that, all else being equal, disease suppression through removal of infected ‘‘INSURANCE’’ POPULATIONS ISOLATED THE DISEASE FROM The observed and foreseeable rapid decline in wild devil distribution and densities gives immediate priority to successfully establishing an ‘‘ark’’ comprising a combination of captive and wild-living ‘‘insurance’’ populations in locations protected from disease. Captive insurance populations, which differ in their risk of developing DFTD (Table 2), include: 1) wildsourced founders and their progeny held at four zoos on mainland Australia (currently 47 devils derived from 25 juvenile founders collected from disease-free areas in 2005 and quarantined for 2 years in Tasmanian government centers, and 2 devils from preexisting mainland captive population); 2) captive-bred devils in Tasmanian Wildlife Parks (most of these parks abut populations containing infected devils); 3) orphans from diseased mothers held in separate facilities in some Tasmanian wildlife parks; and 4) wild-source founders in Tasmanian government quarantine facilities. There may also be potential to establish further insurance populations in international zoos. A detailed protocol is used to select wild-sourced founders to minimize disease risk. Devils are sourced from geographic areas at least 50 km from the known disease front or a low probability of disease at the site established through intensive trapping. Criteria for selection include that a devil must be a subadult of the current annual cohort, as close to weaning age as possible given logistical constraints (devils, primarily males, disperse after weaning), that is reproductively immature (female pouches undeveloped), and without recent or old (scars) penetrating injuries. Quarantine periods are based on a latent period potentially up to 1 year Managing Tasmanian Devil Facial Tumor Disease Table 2. Possible Types of Managed Tasmanian Devil Populations and Their Associated Risks Situation Management intensity Risk of disease outbreak Risk to other species Mainland and international zoos Tasmanian wildlife parks Tasmanian orphans from diseased mothers Free-ranging island populations Fenced peninsulas with disease suppression/eradication Fenced enclosures—Tasmania Fenced enclosures—mainland High High High Low Medium High High Low Medium Medium Low Medium High Low Low Low Low Low–Medium Low Low High (Pyecroft et al., 2007) and the almost complete absence of wild devils over the age of 3 [Lachish et al., in preparation]. A set of biosecurity protocols has been developed to advise operators how to manage animals in each group, based on current knowledge of the disease. Additional problems are the species’ natural life-history constraint of a short reproductive life-span (3 years) and a track record of low reproductive output in captivity (typically <30% of adult females breeding each year). The latter problem needs to be addressed through skills transfer, capacity building, and improved knowledge of the devil’s breeding biology and captive management. Captive ‘‘insurance’’ populations, while necessary, do not meet the goal of maintaining the Tasmanian devil as an ecologically functional species in the wild. Free-ranging populations free of the disease could potentially be established on offshore islands, fenced peninsulas in areas that are still disease-free, or large fenced enclosures. Given the difficulty and cost of constructing and particularly of maintaining long fences (in a forested terrain where trees and branches fall on fences and wombats dig under them), the island possibility is the most attractive from the viewpoint of maintaining disease-free status. Translocation to islands has been extensively used to protect endangered species from introduced predators (Saunders et al., 2006), but rarely to protect a species from disease (although island populations of koalas, Phascolarctos cinereus, were established for that reason in the early 20th century). Generalist predators introduced to islands may adversely affect species that have had no evolutionary exposure to them (Savidge, 1987; Courchamp et al., 2003). To translocate devils to islands, the conservation benefit to the devil must outweigh any threat to other species on the islands. Guidelines recommend caution in translocating species to environments from which they have been historically absent (IUCN, 1987; Anonymous, 1994). No Tasmanian offshore island has supported a natural devil population in historical times, although most Bass Strait islands would have had devils on them when the Bassian Plain flooded 13,000 years ago and sub-fossil remains recovered from Flinders Island are thought to date to the early 1800s (Hope, 1972). Even so, there are no terrestrial vertebrate species on the larger Tasmanian offshore islands that have not already coexisted with devils on mainland Tasmania for thousands of years. A recent meta-analysis indicates that alien predators (e.g., foxes, Vulpes vulpes, and feral cats, Felis catus) are more dangerous than native predators (e.g., devils) to prey populations (Salo et al., 2007). Some species of seabirds, however, select usually smaller islands to nest in predator-free situations. Many Tasmanian offshore islands have had feral cat populations for many decades. Most of Tasmania’s 330 offshore islands (Brothers et al., 2001) are too small or lack enough habitat, food, or water to sustain a functioning Tasmanian devil population. At typical devil densities of 1–2 km)2, even the large Bass Strait islands, King (1,728 km2) and Flinders (1333 km2) and the near-shore southeastern Bruny Island (352 km2) would, on their own, be too small to support a population of devils immune from long-term genetic deterioration (Franklin and Frankham, 1998). However, a metapopulation approach (e.g., Foose et al., 1995), involving strategic exchanges of animals between several island populations and some smaller but more intensively managed captive populations, could be capable of sustaining a long-term, genetically robust insurance population for the species. Without management intervention, extinction from DFTD in about 20 years is possible (McCallum et al., 2007). Successful reintroduction across the species’ range, should this be required, could take more than a decade (Beck et al., 2004). Therefore, a precautionary approach would plan for a metapopulation Menna E. Jones et al. capable of retaining a representative sample of the species’ genetic variation for up to 50 years. For captive insurance populations, retention of 90% of wild source gene diversity is generally considered a reasonable compromise between retaining genetic potential and using financial resources efficiently (Soule et al., 1986). As the insurance metapopulation discussed here could become the sole reservoir of genetic variation for this species, and as devils have low genetic diversity (Jones et al., 2004), more ambitious targets are appropriate. Ideally no loss would be incurred but retention of at least 95% is recommended here. To capture the rare alleles known to be important for long-term adaptive potential (Spielman et al., 2004), a large number of founder animals is required. As a guide, a sample of 30 founders carries a high probability (95%) of retaining in the population those alleles occurring with a frequency of P ‡ 0.05 while capturing those occurring at P ‡ 0.01 could require 150 (Marshall and Brown, 1975). This number of founders would be a sound base for an insurance metapopulation and one which would be expected to capture between 98.3% and 99.67% of wild source genetic diversity (e.g., Frankham et al., 2002). Securing somewhere in between these two figures may be possible in the next 12–24 months before the window for collecting disease-free animals closes, although these wild founders can now only be collected from the northwestern genetic province. While devils are found across Tasmania, landscape features restrict gene flow between the subpopulation in the northwest of the state and the eastern, southern, and southwestern provinces. A strong isolation by distance pattern in genetic differentiation is evident so that devils in the northwest province are genetically distinct from others at the level of a management unit (Moritz, 1994; Jones et al., 2004; Farmer, 2006). Ideally, founders should be sourced from across the species range to capture local adaptive genetic variation (Moritz and Faith, 1998; Moritz, 1999). The founder population of Tasmanian devils should be geographically sourced to represent the east-to-northwest genetic differentiation in the wild devil population (Jones et al., 2004; Farmer, 2006). Currently, the majority of founders in captive populations are of eastern provenance, so a collection of founders from the northwest province is desirable. There will be ongoing opportunity to enhance the founder base with orphans, sourced primarily from eastern provinces, from disease-suppression trials and from roadkill (increasingly rare). Ideally, founders for wild-living island insurance populations should be translocated directly from the wild. Wild animals will bring their entire complement of parasitic, pathogenic, and commensal fauna with them, thus also ensuring the conservation of this fauna. Even holding wild devils for several months in captivity before release on an island will result in population changes in their parasitic fauna. Captive devils live in unnaturally very high densities, and build-up of parasites is likely in both the animals and in the soil of the pens, particularly when the life cycle of the parasite is shorter than the period in captivity. Worming treatment is usually required in this situation which will further alter the parasite community. Protecting the genetic diversity collected for insurance populations in the wild-sourced founders against subsequent genetic drift would require rapid growth to, and subsequent maintenance at, a predetermined target population size (Foose and Ballou, 1988). In the context of retaining genetic diversity, the size of interest is not the absolute but the effective population size (Wright, 1931). This is defined as the size of an ‘‘idealized’’ population that would lose variation at the same rate as the actual population. Real populations deviate in structure from the assumptions of the idealized population by having unequal sex-ratios, highly variable family sizes, fluctuating population size, and overlapping generations (Frankham et al., 2002). Consequently, the effective population size (denoted as Ne) is usually less than the absolute one (denoted as N). Estimates of effective sizes for wild populations average 11% of census size (Frankham, 1995), while in captive populations, values of 20%–50% of census size are typical (Foose and Ballou, 1988). The target population size for the overall insurance population would therefore depend on the planned distribution of the metapopulation between captive and free-ranging populations. The greater the proportion allocated to the latter, the larger the overall metapopulation would need to be in order to compensate for the reduced efficiency of gene-diversity retention in this component. For example, estimates of the effective population size required to maintain evolutionary potential (that is, to achieve no net loss of genetic variation) range from 500 to 1250 (Franklin, 1980; Franklin and Frankham, 1998). Based on the lower of these estimates, and assuming Ne/N ratios of 0.3 for captive devils and 0.1 for free-living ones, a metapopulation based solely on captive populations would require a census size of approximately 1700 individuals, while a genetically equivalent free-ranging Managing Tasmanian Devil Facial Tumor Disease population would need a census size of approximately 5000 to achieve the same genetic objectives. DISEASE SUPPRESSION Selectively removing infected individuals from the population reduces R0 by reducing the opportunity an infected individual has to transmit disease. If R0 is reduced below one (secondary case per primary case) the disease will go extinct. Without a vaccine, ‘‘trap, test, and remove’’ is commonly deployed to control wildlife diseases (e.g., Wolfe et al., 2004). Allograft transmission, which requires transfer of cells from within the tumor of an infected devil through a break in the skin of the recipient, suggests that while infected individuals that have not yet developed a tumor might be infectious, the chance of transmission is probably quite low until a tumor is visible. As the tumors grow larger, they ulcerate and become friable. The likelihood that a bite from another devil will connect with a tumor and that the tumor will shed cells increases with the size and multiplicity of the tumor(s). Infected devils targeted for culling should be removed at as early a tumor stage as possible, before they can infect another devil. Whether disease eradication is achievable depends on the infectivity of the disease, the trapping effort in relation to key transmission periods, the rate of progression of the tumor and stage at which it becomes transmissive, the degree of site isolation (natural; enhanced by fencing), and whether a cryptic (i.e., untrappable) population provides a tumor reservoir. The first adaptive management trial in disease suppression, through selective removal of infected animals, began at the Tasman and Forestier peninsula soon after arrival of the disease. A 12-month pilot study commenced in June 2004, followed by an intensive trial starting in January 2006. Commencing disease control before the pathogen becomes established is a strategy which may increase the trial’s chance of success (Sakai et al., 2001). This large peninsula (360 km2) is connected to mainland Tasmania by a single bridge. All devils seen to be overtly infected or to have characteristic signs considered to precede DFTD (there is no diagnostic test apart from histologically testing a visible tumor) are being removed (and euthanized) in an intensive trapping program (four or five 10-day trips per year) from a 160-km2 area comprising the diseased zone and a buffer. Twelve months of intensive trapping (after 18 months of a less intense study) and Figure 2. Change in the tumor stage of devils removed in the first 12 months of a disease-suppression trial on a large peninsula. Shades of gray represent, from lightest to darkest: devils classified as having characteristic signs considered to precede DFTD, single small tumors (<1 cm diameter), multiple small tumors, single medium-size tumor (1)4 cm), multiple medium tumors, any large tumors (>4 cm). removal have influenced the epidemic’s progress. Fewer large tumors are now being found (X2 = 18.025, df = 8, P = 0.021; Fig. 2) and the population density has remained high (1.6 devils km)2; Jones, unpublished data) compared with a similar site without disease suppression (Freycinet, 160 km2 peninsula also on the east coast: reduction from 0.9 to 0.6 devils km)2 over a similar time frame since arrival of the disease) (McCallum et al., 2007). Alternative methods of disease suppression (to removal of infected individuals) include, in ascending order of initial population impact: removal of selected population classes or individuals, removal of all adults, and removal of healthy individuals to reduce population density. Selective removal of individuals or population classes might be an effective strategy if such animals are shown to be ‘‘superspreaders,’’ particularly if times of the year were targeted when transmission is particularly high, such as just prior to the mating season. At diseased sites with severely reduced populations, removing all of the very few remaining adults (the age-class likely to be overtly diseased; Lachish et al., 2007) immediately after they have weaned their young may be an acceptable and effective means of rapidly limiting disease prevalence, potentially even achieving rapid eradication. This strategy would leave the current cohort of recently weaned juveniles (9 months old) to reestablish the population. DFTD has not been observed in subadults younger than 13 months and is rarely observed under 20 months (Hawkins et al., in preparation). The effectiveness Menna E. Jones et al. of this strategy will also be influenced by the latent period, estimates for which are currently about 6 months (Pyecroft et al., 2007). Reducing population density to reduce disease transmission is unacceptable for use with endangered wildlife, and inappropriate for a frequency-dependent disease, although frequently used to control infectious livestock diseases. Even then it can be counterproductive, resulting in disruption to social structures, an increase in movements with subsequent increase in disease transmission (Donnelly et al., 2003). With all disease-suppression options, the disease control benefits of removing individuals from the population need to be weighed against the future reproductive value of the individuals removed. Possible outcomes of disease-suppression trials are: 1) failure to influence the demographic consequences of the disease epidemic; 2) the maintenance of an intact highdensity, age-structured population but with DFTD still present; or 3) an intact population with the disease eradicated. A trigger point that would indicate failure of the trial would be if the age structure of the population became statistically indistinguishable from that of a population in which the disease was not controlled (e.g., Lachish et al., in preparation). If populations can be protected through disease suppression, they can be harvested to contribute, through genetic exchange, to other components of the insurance metapopulation. Animals selected for ‘‘migration’’ would have a higher level of risk of carrying DFTD than captive or island populations and would need to be quarantined accordingly. In the event of outcome 2), the disease risk would be high; the same as for current broadscale diseased populations. Disease suppression does offer currently the only possibility for maintaining ecologically functional devil populations where the disease is present on mainland Tasmania. ECOSYSTEM CONSEQUENCES The removal of strongly interactive top predators from an ecosystem predictably results in: 1) mesopredator release, an increase in abundance of smaller predators previously suppressed by the top carnivore and consequent decreased abundance of their prey; 2) prey release, an increase in abundance of prey of the top carnivore and consequent increased consumption of plant species by released herbivorous prey; and 3) changes in ecosystem function through changes in community composition, productivity, and stability (Schmitz et al., 2000; Switalski, 2003; Gehrt Figure 3. Tasmania-wide trends in abundance of Tasmanian devils (solid circles) and feral cats (open circles) observed during standard annual spotlight transect counts [Greg Hocking, unpublished data] and in hard evidence of foxes (open squares) recorded from 1995, which was prior to the emergence of devil facial tumor disease, to 2006. and Prange, 2007), including in mainland Australian ecosystems (Glen and Dickman, 2005; Mitchell and Banks, 2005; Johnson et al., 2006, 2007). Since the extinction of the thylacine, Thylacinus cynocephalus, in the 1930s and likely disruption of predator–prey relationships, the devil has been the largest predator in Tasmania. Predicting ecosystem consequences of DFTD-induced decline is complicated by the recent impending establishment of red foxes in Tasmania, albeit in low numbers so far (Mooney, 2004; Saunders et al., 2006) (Fig. 3). Given the known diet of devils (Guiler, 1970; Jones and Barmuta, 1998), their specialized scavenging role (Jones, 2003), and relationships among devils and the next smaller native carnivores, the spotted-tailed quoll, Dasyurus maculatus, and eastern quoll, D. viverrinus (Jones, 1997; Jones and Barmuta, 1998, 2000), we expect densities of macropod prey and spotted-tailed quolls to increase as devils decline, and carrion to persist in the landscape. Anecdotal evidence vindicates these predictions: browsing impact and spottedtailed quolls are increasing and carcasses now persist longer. Alternative scavengers such as forest ravens, Corvus tasmanicus, may increase, with possible impacts on populations of bush birds on whose eggs and nestlings ravens prey. Where spotted-tailed quoll densities rise, densities of the smaller eastern quoll are likely to fall. As there is limited overlap in the core distributions (Jones and Rose, 1996) and habitat preferences (Jones and Barmuta, 2000) of these two species, suppression of eastern quolls is likely to occur Managing Tasmanian Devil Facial Tumor Disease only in limited areas. The two species could become even further separated by habitat. Devils may previously have suppressed feral cat densities (and their impact on native wildlife) and previous fox incursions in Tasmania, most likely through interference competition (Macdonald and Thom, 2001), either aggressive exclusion or predation by devils upon kittens and cubs. Monitoring evidence suggests that an increase in cats has begun (Fig. 3). Devil decline may allow foxes to increase and threaten wildlife as they have in mainland Australia (Burbidge and McKenzie, 1989; Cardillo and Bromham, 2001). The seriousness of the fox threat, to wildlife and to the sheep industry, has been recognized by government through the establishment of the fox eradication program. If eradication fails and dense fox populations develop, eventual reestablishment of wild devil populations will be much harder as foxes are likely also to prey on devil cubs necessarily left unattended in dens while the female forages. DISCUSSION The most likely short-term outcome of the devil facial tumor disease epidemic is a patchy mosaic of local extinctions of devils and local persistence of devil populations but with the disease (Table 1). Given any of the possible scenarios, most Tasmanian ecosystems will almost certainly lose the ecological functionality of the devil. That functionality is highly unlikely to be restored without careful management started now and planned for the medium and long term. A whole-ecosystem approach to managing the changes in predator dynamics in Tasmania needs a substantial increase in effort towards fox eradication and feral cat suppression. The loss of devils will otherwise predictably enable these feral predators to increase and subsequently to exert increased predatory pressure on medium-sized prey species. The ecosystem consequences of the loss of the devil include an increased extinction threat to many species of mammals that have declined catastrophically in southern mainland Australia since fox and cat introductions, but which persist in Tasmania. These include the eastern quoll, the Tasmanian bettong, Bettongia gaimardi, the Tasmanian Pademelon, Thylogale billardierii, and the Eastern Barred Bandicoot, Perameles gunnii (Museum of Victoria http://www.flyaqis.museum.vic.gov.au/cgi-bin/texhtml). The flightless, endemic Tasmanian native-hen, Gallinula mortierii, would also be severely threatened. The time scales for natural evolution of resistance to DFTD, for genetic management (artificial selection for resistance), or for development of a field-deliverable vaccine are too long and the likelihood of positive outcomes too uncertain to rely on these to secure the future of the devil. Shorter-term management actions are limited to establishing a ‘‘insurance’’ populations protected from the disease. These need to be managed as a metapopulation with the goal of maintaining a conservative level (95%) of the genetic diversity of the species for about 50 years in the event that regional extinction of devils and DFTD allows reintroduction. Management actions currently available that might achieve this objective are the establishment of captive and wild-living island populations isolated from the disease, and disease suppression through removal of infected devils in areas that can be isolated with the goal of eradication. The former currently provide a higher security from DFTD than disease suppression. The first adaptive management trial in disease suppression is underway, some captive populations have already been established, and the establishment of further captive and island insurance populations is achievable now, pending stakeholder support. What should be the relative roles of captive and island insurance populations in the ‘‘ark’’? The advantages of captivity are the ability to manage and monitor genetic and demographic outcomes closely, high biosecurity, and the need for a smaller effective and thus actual population size. The disadvantage is cost; captive management is expensive, labor intensive, and requires careful coordination to be effective. The operating costs of free-ranging populations are considerably lower but with a lower effective-to-actual population size ratio (Ne/N), larger population sizes are required to achieve equivalent genetic and demographic goals (Ballou and Lacy, 1995; Frankham, 1995). However, wild-living populations have several advantages over captive insurance populations. First, each island, if carefully chosen, could hold more devils than any captive population; starting with a much larger founder group is cheaper and more desirable than attempting to rectify low genetic diversity at a later stage (Ballou et al., 1995). Second, wildliving devils will retain natural behaviors, as they are not subject to the selective forces of captive conditions but hunt, live under predation risk, and choose mates naturally. This means they are better adapted to the wild, are more suitable for reintroduction, and should more closely represent the species’ phenotypic potential. Third, wildliving populations retain their natural suite of parasitic, Menna E. Jones et al. pathogenic, and commensal fauna which might be lost in captive devils routinely treated with prophylactic antiparasitic drugs. Free-living insurance populations thus also militate against the extinction of this fauna. It is important to maintain several spatially separated captive, and several spatially and ecologically separated wild-living, insurance populations as protection against catastrophic stochasticity or disease introduction (whether inadvertent or deliberate). Captive and island insurance populations do not assist in maintaining ecological functionality within the devil’s historic range on the Tasmanian mainland, although there is benefit to be derived from suppression of macropod populations on some islands, where they are regularly culled to prevent overpopulation. How much of the landscape of mainland Tasmania where the disease is established can be protected using current tools, either disease suppression or fencing off large areas that are currently disease-free? Broadscale disease suppression, including halting the spread of the disease into western Tasmania and even intentional eradication of devils on the Tasmanian mainland, is probably not feasible even with unlimited resources. We are trying to manage a cryptic, nocturnal, largely solitary wild species and vast areas of inaccessible wilderness through which the disease is spreading. Establishing a depopulated ‘‘cordon sanitaire’’ to protect the currently disease-free northwest would require aerial distribution of poison baits. Those currently available are not species-specific, can not be acceptably used with a threatened species, would lead to non-target deaths, and could actually increase devil movement and disease transmission (e.g., badger culling; Donnelly et al., 2003). Even on peninsulas that can be isolated, disease suppression has ongoing costs, and these will increase with the length of fencing required to enhance natural water barriers. If eradication can be achieved or if a large currently disease-free area (preferably a peninsula) was fenced, the costs of monitoring the disease status of peninsula populations will still be higher than costs of monitoring island populations; stretches of ocean provide a higher level of biosecurity against natural movement of devils than fencing. Fencing of a peninsula has been used successfully to protect native mammals from feral cat predation in Western Australia (Short and Turner, 2005). However, incursions of cats into a cat free peninsula are much more readily detectable than incursions of diseased (but possibly asymptomatic) devils into a peninsula already containing devils. Further, any secondary infection that occurred following such an incursion would not be detectable or removable until after the (as yet unknown) latent period of the disease. Thus, protecting large areas of mainland Tasmania from the disease to maintain ecological functionality would have very large, ongoing costs. These costs need to be balanced against the benefits of maintaining the devil as an ecologically functional species in the landscape. Benefits of devils, variously to conservation and/or livestock farmers, potentially include suppression of feral foxes and cats, suppression of macropod and possum populations that are culled in some areas, and ecological services to livestock farmers such as cleaning up carcasses and reducing rates of blowfly strike of sheep. All of these benefits also need to be balanced against the costs to the farmer of lamb predation by devils and foxes. Finally, the responsible authorities need to be aware that devil conservation will need active management for decades to mitigate the disease’s manifold effects. We need a commitment to resource the program financially, beyond the life of governments and even the careers of the biologists, until such time as this iconic species has been removed from threatened species lists. ACKNOWLEDGMENTS We thank Stephen Pyecroft, Alex Schaap, John Whittington, Barrie Wells, Rupert Woods, and Steven Smith who have contributed to the ideas in this document; Greg Hocking for the provision of spotlighting data; and Marco Restani for collaboration. We are very grateful to the numerous individuals who have helped with captive and wild management. For captive management, we are grateful to the trappers, keepers, and veterinarians who collected and maintain the Tasmanian government quarantine populations, especially James Harris for veterinary services; the owners, managers, and keepers of all of the Tasmanian Wildlife Parks and four mainland Australian zoos; and Qantas for transporting devils to the mainland. We are indebted in so many ways to the Dunbabin family (Tom, Cynthia, and Matthew), on whose land we conducted the disease-suppression trial; to John Hamilton for trialing devil-proof road grids and housing orphan devils; to Jim Platt for road engineering to secure the peninsula; and to the wildlife carers who raise the orphans. We thank Richard Koch (Parks and Wildlife Service) for assistance with developing island plans. The trapping and captive Managing Tasmanian Devil Facial Tumor Disease programs could not function without countless hours put in by large numbers of volunteers. 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