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Australia’s mammal fauna requires a strategic and enhanced network of predator-free havens

© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Australia’s mammal fauna requires a strategic
and enhanced network of predator-free havens
To the Editor — Introduced cats (Felis catus)
and European red foxes (Vulpes vulpes)
have caused the precipitous decline and
extinction of many native mammal species
in Australia1. Many surviving species now
persist in the wild only on predator-free
islands and in small natural refugia where
introduced predators are at low density.
These natural refugia have inspired the
creation of ‘safe havens’: areas where
populations of imperilled mammals can be
protected from introduced predators, either
on offshore islands, or by predator-proof
fences on the mainland2.
The creation of safe havens
revolutionized Australian mammal
conservation in the late twentieth century.
The number of these havens has increased
rapidly over the past 30 years (Fig. 1);
there are now 17 fenced areas (with a
further seven under construction) as
well as 22 islands on which introduced
predators have been eradicated and where
populations of native mammals have been
translocated and established. Introduced
predator eradications are currently
planned for five more large Australian
islands. These havens have improved the
population status and probably prevented
the extinction of some of Australias most
imperilled mammal species, mostly species
of arid and semi-arid distribution, and
larger body size. The network currently
protects 38 mammal taxa regarded
as highly or extremely susceptible to
predation from introduced predators.
Most havens have been created
by governments, non-government
organizations and private landholders
acting largely independently of each
other. Under a decentralized governance
structure, and without an explicitly unified
objective, new havens risk being established
inefficiently, as seen in the early growth of
protected area networks3,4. For example,
although the 11 havens created over the
past seven years increased protection for
16 predator-susceptible taxa, these were
already represented in the haven network
and no unrepresented taxa were added to
the network (Fig. 1). Twenty-nine predator-
susceptible taxa remain unrepresented in the
haven network. If a primary conservation
objective is to ensure comprehensive
protection for all at-risk species, current
expansion is performing poorly.
If national scale objectives such as
adequate representation of all predator-
susceptible taxa in havens are to be met
efficiently, new havens need to address
representation gaps in the existing network.
Systematic conservation prioritization
methods5 can help to identify the best
locations for new havens, and inform
strategies for determining the order in which
taxa are added to the network. However,
successful application of these tools requires
conservation action to be coordinated and
communicated among the conservation
actors who contribute to the haven network.
This will be difficult to achieve because
the actors are diverse and employ different
models to fund conservation actions6.
Ultimately, the success of the haven network
Safe haven creation date
Taxa protected (%)
Number of safe havens
Fig. 1 | Increase in species representation under haven network expansion. a, Representation of predator-
susceptible taxa in havens compared with growth in havens since 1990. Black line, percentage of taxa
protected by havens over time for a national target of 67 predator-susceptible taxa; blue line, number of
safe havens over time. The pink band indicates the 11 havens created over the past seven years, which have
only provided coverage for previously represented species. b, A greater bilby (Macrotis lagotis). Bilbies
have been a primary focus for Australian havens. Credit: b, Dave Watts/Alamy Stock Photo.
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved. © 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
will be judged by its capacity to sustain all
predator-susceptible taxa until eradication
of introduced predators on landscape or
national scales becomes viable, allowing
re-introduction outside havens. This
goal is achievable if decisions are informed
by a coordinated national strategy
supported by state-of-the-art conservation
planning approaches.
Jeremy Ringma1,2,3*, Sarah Legge2,4,
John Woinarski5, Jim Radford6,
Brendan Wintle7 and Michael Bode8
1School of Biological Sciences, e University of
Western Australia, 35 Stirling Highway, Crawley,
Western Australia 6009, Australia. 2Centre for
Biodiversity and Conservation Science, University
of Queensland, St Lucia, Queensland 4072,
Australia. 3Department of Natural Resources and
Environmental Management, e University of
Hawai‘i, Manoa, HI 96822, USA. 4Fenner School
of Environment and Society, e Australian
National University, Canberra, Australian Capital
Territory 2601, Australia. 5Research Institute for
the Environment and Livelihoods, Charles Darwin
University, Casuarina, Northern Territory 0909,
Australia. 6Research Centre for Future Landscapes,
School of Life Sciences, La Trobe University,
Victoria 3083, Australia. 7University of Melbourne,
Melbourne, Victoria 3010, Australia. 8ARC Centre
of Excellence for Coral Reef Studies, James Cook
University, Townsville, Queensland 4811, Australia.
Published: xx xx xxxx
1. Woinarksi, J. e Action Plan for Australian Mammals
(CSIRO, Collingwood, 2012).
2. Haywards, M. & Somers, M. (eds) Fencing for Conservation:
Restriction of Evolutionary Potential or a Riposte to reatening
Processes? (Springer, New York, 2012).
3. Pressey, R. & Madeleine, B. Conserv. Biol. 22,
1340–1345 (2008).
4. Ringma, J. et al. Conserv. Biol. 31, 1029–1038 (2017).
5. Margules, C. & Pressey, R. Nature 405, 243–253 (2000).
6. Iacona, G., Bode, M. & Armsworth, P. Conserv. Biol. 30,
1245–1254 (2016).
This research was supported by the Australian
government’s National Environmental Science
Program, through the Threatened Species
Recovery Hub.
Competing interests
The authors declare no competing financial interests.
... Conservation interventions can also indirectly affect behavioural responses in target species. Common strategies employed to prevent faunal extinctions include captive breeding [26], translocations (the deliberate movement of animals from one population or site for release in another [27]), and establishment of populations in predator-free havens (areas isolated from predators through a geographical or physical barrier, such as islands or fenced enclosures [28][29][30]). Such approaches have secured a number of populations of mammals, including African elephants [31,32], European lynx [33], elk [34], giant pandas [35], and Tasmanian devils [36]. ...
... More than one third of modern mammal extinctions have occurred in Australia, largely due to the introduction of feral cats and foxes [37]. In response, havens free of introduced predators are a key component of conserving much of the remaining mammal fauna [29,30,38]. Australia's current network of havens provides habitats for at least 32 mammal species, and has secured at least 188 populations and sub-populations [29]. ...
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Background Mammals, globally, are facing population declines. Protecting and breeding threatened populations inside predator-free havens and translocating them back to the wild is commonly viewed as a solution. These approaches can expose predator-naïve animals to predators they have never encountered and as a result, many conservation projects have failed due to the predation of individuals that lacked appropriate anti-predator responses. Hence, robust ways to measure anti-predator responses are urgently needed to help identify naïve populations at risk, to select appropriate animals for translocation, and to monitor managed populations for changes in anti-predator traits. Here, we undertake a systematic review that collates existing behavioural assays of anti-predator responses and identifies assay types and predator cues that provoke the greatest behavioural responses. Methods We retrieved articles from academic bibliographic databases and grey literature sources (such as government and conservation management reports), using a Boolean search string. Each article was screened against eligibility criteria determined using the PICO (Population–Intervention–Comparator–Outcome) framework. Using data extracted from each article, we mapped all known behavioural assays for quantifying anti-predator responses in mammals and examined the context in which each assay has been implemented (e.g., species tested, predator cue characteristics). Finally, with mixed effects modelling, we determined which of these assays and predator cue types elicit the greatest behavioural responses based on standardised difference in response between treatment and control groups. Review findings We reviewed 5168 articles, 211 of which were eligible, constituting 1016 studies on 126 mammal species, a quarter of which are threatened by invasive species. We identified six major types of behavioural assays: behavioural focals, capture probability, feeding station, flight initiation distance, giving-up density, and stimulus presentations. Across studies, there were five primary behaviours measured: activity, escape, exploration, foraging, and vigilance. These behaviours yielded similar effect sizes across studies. With regard to study design, however, studies that used natural olfactory cues tended to report larger effect sizes than those that used artificial cues. Effect sizes were larger in studies that analysed sexes individually, rather than combining males and females. Studies that used ‘blank’ control treatments (the absence of a stimulus) rather than a treatment with a control stimulus had higher effect sizes. Although many studies involved repeat measures of known individuals, only 15.4% of these used their data to calculate measures of individual repeatability. Conclusions Our review highlights important aspects of experimental design and reporting that should be considered. Where possible, studies of anti-predator behaviour should use appropriate control treatments, analyse males and females separately, and choose organic predator cues. Studies should also look to report the individual repeatability of behavioural traits, and to correctly identify measures of uncertainty (error bars). The review highlights robust methodology, reveals promising techniques on which to focus future assay development, and collates relevant information for conservation managers.
... Conservation managers in Australia, and particularly Western Australia, have been proactive in undertaking conservation translocations (Short, 2009), with some schemes in operation for more than 30 years (Morris et al., 2015;Richards, 2012). Across Australia, predator-free mainland enclosures and island safe havens contribute substantially to the conservation of a suite of native mammal species now otherwise extinct on the mainland-including boodies (Bettongia lesueur), greater stick nest rats (Leporillus conditor), mala (Lagorchestes hirsutus) and the Shark Bay (formerly 'western barred') bandicoot (Perameles bougainville) Ringma et al., 2018). ...
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Translocation programmes are increasingly being informed by genetic data to monitor and enhance conservation outcomes for both natural and established populations. These data provide a window into contemporary patterns of genetic diversity, structure and relatedness that can guide managers in how to best source animals for their translocation programmes. The inclusion of historical samples, where possible, strengthens monitoring by allowing assessment of changes in genetic diversity over time and by providing a benchmark for future improvements in diversity via management practices. Here, we used reduced representation sequencing (ddRADseq) data to report on the current genetic health of three remnant and seven translocated boodie ( Bettongia lesueur ) populations, now extinct on the Australian mainland. In addition, we used exon capture data from seven historical mainland specimens and a subset of contemporary samples to compare pre‐decline and current diversity. Both data sets showed the significant impact of population founder source (whether multiple or single) on the genetic diversity of translocated populations. Populations founded by animals from multiple sources showed significantly higher genetic diversity than the natural remnant and single‐source translocation populations, and we show that by mixing the most divergent populations, exon capture heterozygosity was restored to levels close to that observed in pre‐decline mainland samples. Relatedness estimates were surprisingly low across all contemporary populations and there was limited evidence of inbreeding. Our results show that a strategy of genetic mixing has led to successful conservation outcomes for the species in terms of increasing genetic diversity and provides strong rationale for mixing as a management strategy.
... To help recover the species, the Australian Wildlife Conservancy (AWC) planned multiple translocations into fenced reserves across the species' former distribution and will manage the species as a metapopulation ongoing. In Australia, fenced reserves provide a 'safe haven' for species vulnerable to fox and cat predation to recover without the threat of predation, providing important source populations for future efforts to recover the species beyond the fence as well [25,26]. To increase the species' resilience to climate change, a key component of managing adaptive capacity is exposing the species to the range of former environmental conditions experienced prior to the population decline, as well as maintaining genetic diversity within and across sites. ...
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The application of genetic data to conservation management programs can be hindered by the mismatch in timelines for management decisions and the acquisition of genetic data, particularly genomic sequence data that may require outsourcing. While applying genetic principles where data are absent can provide general guidelines for actions, genetic data can often fine-tune actions through adaptive management. We describe the adaptive genetic management of the establishment of a metapopulation of a small arboreal marsupial, the red-tailed phascogale (Phascogale calura). Two captive breeding programs were established as source populations, with genetic principles applied to the establishment of the first program and empirical genetic data used to guide the establishment of the second program. Genetic data from both programs were then used to allocate founders to three new populations to create a metapopulation with diversity both within and among the sites. Building and maintaining the diversity of metapopulations when recovering threatened species will reduce pressure on the original source populations and increase the resilience of the species.
... These two threatened rodent species have subsequently benefited from recent translocations to islands without introduced predators, and to predator exclosures in mainland settings . However, such translocations have been attempted for far fewer threatened rodent than marsupial species (Ringma et al. 2018), perhaps because there may be less public appeal for rodents and/or because the relatively small body size of most threatened rodent species may mean they are not readily enclosed within predator exclosure fencing. ...
... These two threatened rodent species have subsequently benefited from recent translocations to islands without introduced predators, and to predator exclosures in mainland settings . However, such translocations have been attempted for far fewer threatened rodent than marsupial species (Ringma et al. 2018), perhaps because there may be less public appeal for rodents and/or because the relatively small body size of most threatened rodent species may mean they are not readily enclosed within predator exclosure fencing. ...
Populations of threatened animals are increasingly preserved within predator-free havens, where populations tend to grow rapidly, resource competition increases, and traits relevant to avoiding predation may be selected against. We examine this phenomenon using a ten-year longitudinal dataset on a threatened Australian mammal; the woylie (Bettongia penicillata ogilbyi). Behavioural and morphological data were collected during routine monitoring of a havened woylie population and an adjacent wild population where predators occur, from which six traits relating to predator escape were extracted. Paired comparisons revealed that havened woylies were less likely to show injuries from excessive agitation in traps, were less likely to eject pouch young, and had shorter approach distances compared to woylies outside the haven, suggesting a dampened antipredator response. Further, body mass and relative leg length declined over time in the havened population, compared with no change outside of the haven, suggesting selection in the haven against body size. Population density affected body size and agitation in traps differently in havened and non-havened populations, indicating an interaction between resource competition and relaxed selection that likely hastens the loss of anti-predator traits. Our study offers a mechanistic understanding of the loss of anti-predator responses in havens, which is essential for guiding how populations could be managed to better realise their potential for recovering threatened fauna.
The Australian marsupial fauna has been devastated in the past 250 years, mainly due to impacts from invasive mammalian predators (cats and foxes), although other threats such as invasive herbivores, habitat loss and fragmentation, changes to fire regimes, and now climate change have played a role. The profound and ongoing impact of invasive predators has driven substantial research and management innovation. Australia has been at the forefront of developing approaches to reduce the density and impacts of introduced predators and implementing novel and ambitious species conservation programs. A large and growing network of islands and mainland fenced areas, free of introduced predators (“havens”), has been critical for avoiding further species extinctions. Outside these havens, advances in toxin presentation and deployment have enabled cat and fox densities to be reduced over large areas. Substantial research and field trials have been carried out to understand how predator-prey interactions, and habitat quality management, can be used to reduce predation impacts on susceptible native species. Synthetic biology offers new opportunities to manage introduced predators, including potentially by using gene drives. Finally, the attenuation of the formerly large continuous ranges of many species to small, isolated population remnants (because of predation or other reasons) has also driven research and improvements in genetic and metapopulation management that will increase the chance of population persistence in the longer term. However, unless Australia continues to invest in research and innovative conservation actions, the plight of its priceless marsupial fauna will remain perilous.
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European rabbits (Oryctolagus cuniculus) are ubiquitous across Australia and have the ability to influence native species directly and indirectly. Despite this, limited research focuses on interspecific interactions between rabbits and native mammals. We aimed to determine how site occupancy, detection probability, and temporal activity periods of native mammals changed in response to the presence or absence of rabbits. We monitored three native mammal species using 85 camera traps in a systematic grid at Mt Rothwell Conservation and Research Reserve (Victoria, Australia), a predator‐barrier fenced reserve with two distinct sections—an area with rabbits and an area without. Bettongs (rufous Aepyprymnus rufescens and eastern Bettongia gaimardi), eastern barred bandicoots (Perameles gunni), and southern brown bandicoots (Isoodon obesulus) had a naïve site occupancy of 71%, 42%, and 24%, respectively. Site occupancy for both bandicoot species decreased in areas with more clumping grass with eastern barred bandicoot occupancy increasing with leaf litter cover, and southern brown bandicoots with vegetation height. Rabbit presence did not influence site occupancy of any species. Species detection probabilities were generally positively associated with open vegetation and rabbit presence, except for southern brown bandicoots which were more detectable without rabbits. Both bandicoot species shifted their peak activity periods in the absence of rabbits having an earlier, and more defined activity peak. Our results demonstrate that the presence of rabbits in the absence of invasive predators may not influence the site occupancy of co‐occurring native mammals, however, could influence the behaviour of smaller co‐occurring mammals, either directly or indirectly.
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Conservation fences are an increasingly common management action, particularly for species threatened by invasive predators. However, unlike many conservation actions, fence networks are expanding in an unsystematic manner, generally as a reaction to local funding opportunities or threats. In a gap analysis of Australia's substantial predator exclusion fence network, we found highly uneven protection, with 67% of predator-sensitive species remaining unrepresented. Predator exclusion fences all contain small populations of threatened species, therefore a novel systematic prioritization method for expanding fence networks that explicitly incorporates population viability analysis and minimises expected species’ extinctions was developed. The approach was applied to New South Wales, Australia, where the state government intends to expand the existing conservation fence network. A systematic prioritisation yields substantial efficiencies, reducing the expected number of species extinctions as much as 17 times more effectively than ad hoc approaches. This dramatically superior outcome emphasises the importance of governance when management action is applied in multiple instances with similar objectives and using systematic methods rather than expanding networks opportunistically. This article is protected by copyright. All rights reserved
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The realization of conservation goals requires strategies for managing whole landscapes including areas allocated to both production and protection. Reserves alone are not adequate for nature conservation but they are the cornerstone on which regional strategies are built. Reserves have two main roles. They should sample or represent the biodiversity of each region and they should separate this biodiversity from processes that threaten its persistence. Existing reserve systems throughout the world contain a biased sample of biodiversity, usually that of remote places and other areas that are unsuitable for commercial activities. A more systematic approach to locating and designing reserves has been evolving and this approach will need to be implemented if a large proportion of today's biodiversity is to exist in a future of increasing numbers of people and their demands on natural resources.
To counteract global species decline, modern biodiversity conservation engages in large projects, spends billions of dollars and engages many organizations working simultaneously within regions. To add to this complexity, the conservation sector has hierarchical structure, where conservation actions are often outsourced by funders (foundations, government, etc.) to local organizations that work on-the-ground. In contrast, conservation science usually assumes that a single organization makes resource allocation decisions. This discrepancy calls for theory to understand how the expected biodiversity outcomes change when interactions between organizations are accounted for. Here, we used a game theoretic model to explore how biodiversity outcomes are affected by vertical and horizontal interactions between three conservation organizations: a funder that outsourced its actions, and two local conservation organizations that work on-the-ground. Interactions between the organizations changed the spending decisions made by individual organizations, and thereby the magnitude and direction of the conservation benefits. We showed that funders would struggle to incentivize recipient organizations with set priorities to perform desired actions, even when they control substantial amounts of the funding and employ common contracting approaches to enhance outcomes. Instead, biodiversity outcomes depended on priority alignment across the organizations. Conservation outcomes for the funder were improved by strategic interactions when organizational priorities were well aligned, but decreased when priorities were misaligned. Meanwhile, local organizations had improved outcomes regardless of alignment due to additional funding in the system. Given that conservation often involves the aggregate actions of multiple organizations with different objectives, strategic interactions between organizations need to be considered if we are to predict possible outcomes of conservation programs or costs of achieving conservation targets. This article is protected by copyright. All rights reserved.
The conflict between increasing human population and biodiversity conservation is one of the IUCN’s key threatening processes. Conservation planning has received a great deal of coverage and research as a way of conserving biodiversity yet, while theoretically successful, it has never been tested. Simple lines on maps to illustrate conservation areas are unlikely to be successful in the light of human encroachment. It may be that some form of overt display is necessary to ensure the protection of reserves. This may be signage, presence of guards/rangers or physical fencing structures. The need for some form of barrier goes beyond restricting human access. The megafauna of Africa pose a genuine threat to human survival. In southern Africa, fences keep animals in and protect the abutting human population. Elsewhere, fencing is not considered important or viable. Where poverty is rife, it won’t take much to tip the balance from beneficial conservation areas to troublesome repositories of crop-raiders, diseases and killers. Conversely, in New Zealand fences are used to keep animals out. Introduced species have decimated New Zealand’s endemic birds, reptiles and invertebrates, and several sites have been entirely encapsulated in mouse-proof fencing to ensure their protection. Australia faces the same problems as New Zealand, however surrounds its national parks with cattle fences. Foxes and cats are free to enter and leave at will, resulting in rapid recolonisation following poisoning campaigns. How long will these poison campaigns work before tolerance, aversion or resistance evolves in the introduced predator populations? © Springer Science+Business Media, LLC 2012. All rights reserved.
The Action Plan for Australian Mammals (CSIRO
  • J Woinarksi
Woinarksi, J. The Action Plan for Australian Mammals (CSIRO, Collingwood, 2012).
  • R Pressey
  • B Madeleine
Pressey, R. & Madeleine, B. Conserv. Biol. 22, 1340-1345 (2008).
  • J Ringma
Ringma, J. et al. Conserv. Biol. 31, 1029-1038 (2017).
  • G Iacona
  • M Bode
  • P Armsworth
Iacona, G., Bode, M. & Armsworth, P. Conserv. Biol. 30, 1245-1254 (2016).