Download Conservation Management of Tasmanian Devils

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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