Reintroduction of Tasmanian Devils to Mainland Australia Can Restore Top-Down Control in Ecosystems Where Dingoes Have Been Extirpated

Biological Conservation 191 (2015) 428–435

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Biological Conservation

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Reintroduction of Tasmanian devils to mainland Australia can restore top-down control in ecosystems where dingoes have been extirpated

Daniel O. Hunter a,⁎,ThomasBritzb, Menna Jones c,MikeLetnica a Centre for Ecosystem Science, University of New South Wales, NSW 2052, Sydney, Australia b School of Mathematics and Statistics, University of New South Wales, NSW 2052, Sydney, Australia c Department of Zoology, University of Tasmania, Tasmania 7001, Hobart, Australia article info abstract

Article history: Restoring missing ecological interactions by reintroducing locally extinct species or ecological surrogates for ex- Received 16 February 2015 tinct species has been mooted as an approach to restore ecosystems. Australia's apex predator, the dingo, is sub- Received in revised form 21 July 2015 ject to culling in order to prevent attacks on livestock. Dingo culling has been linked to ecological cascades Accepted 24 July 2015 evidenced by irruptions of herbivores and introduced mesopredators and declines of small and medium sized Available online xxxx mammals. Maintenance of dingo populations is untenable for land-managers in many parts of Australia owing to their depredations on livestock. However, it may be possible to fill the apex predator niche with the Tasmanian Keywords: Rewilding devil which has less impact on livestock. Devils once occurred throughout Australia, but became extinct from the Trophic cascades mainland about 3000 years ago, but are now threatened by a disease epidemic in Tasmania. To explore the fea- Predator diversity sibility of reintroducing devils to mainland Australia we used species distribution models (SDMs) to determine Tasmanian devils if suitable climatic conditions for devils exist and fuzzy cognitive mapping (FCM) to predict the effects of devil Dingoes reintroduction. Based on devils' current distribution, our SDM indicates that suitable areas for devils exist in south-eastern Australia. Our FCM examined ecosystem responses to predator-management scenarios by manipulating the abundances of devils, dingoes and foxes. Our FCMs showed devils would have cascading effects similar to, but weaker than those of dingoes. Devil introduction was linked to lower abundances of introduced mesopredators and herbivores. Abundances of small and medium sized mammals and understorey vegetation complexity increased with devil introduction. However, threatened species vulnerable to fox predation benefited little from devil introduction. Our study suggests that reintroducing ecological surrogates for apex predators may yield benefits for biodiversity conservation. © 2015 Elsevier Ltd. All rights reserved.

1. Introduction (Donlan et al., 2006). Reintroducing strongly interactive species may also be desirable to curb the effects of invasive species, or to ﬁll vacant All species interact with other species both directly and indirectly, niches in novel ecosystems that are dominated by suites of invasive through mechanisms such as predation, competition, mutualism, facili- species. tation and herbivory. The outcomes of such interactions are among the Large carnivores are often keystone species because they typically major factors that shape ecological communities. Species are described occur at low densities and may exert top-down control on ecosystems as strongly interactive when their absence leads to signiﬁcant changes through their predatory and competitive interactions with herbivores in ecosystems and as keystone species when the strength of their inter- and smaller predators (Ripple et al., 2014). Because top predators kill actions is disproportionate to their abundance (Soule et al., 2003). their prey and frequently kill their competitors as well, the most obvious Increasingly, ecologists are realizing that the effects of strongly inter- population-level effects of top-predator removal are increases in the active species could be used to manipulate ecological processes and abundance of large herbivores and smaller predators (mesopredators) achieve biodiversity conservation goals (Seddon et al., 2014; Ritchie (Ripple et al., 2014). et al., 2012). Understanding the important role that strongly interactive While the direct predatory effects of top predators are relatively species can play in shaping ecosystems has prompted debate about the easily observed, they typically have strong indirect effects as well. For merits of restoring missing ecological interactions by reintroducing lo- example, numerous studies have found that, in the absence of a top- cally extinct species or ecological surrogates for now extinct species predator, herbivores increase in abundance, reducing the biomass of palatable plants (Ripple et al., 2014). A similar cascade of effects is predicted by the mesopredator release hypothesis (MRH). The MRH ⁎ Corresponding author at: Daniel Hunter, School of BEES, University of NSW, Kensington, NSW 2052, Australia. postulates that reduced abundance of top-order predators results in E-mail address: [email protected] (D.O. Hunter). an increase in the abundance and predatory impact of smaller predators

(Soulé et al., 1988). Consequently, small prey species that are the one of the reasons why small and medium sized native mammals are so preferred prey of mesopredators may decline in abundance (Prugh abundant there today (Johnson, 2006). et al., 2009). Owing to the amplified interactions of herbivores and Importantly, devils are not as great a threat to livestock as are mesopredators, terrestrial ecosystems from which apex predators dingoes, although their predatory impact is at least similar to that of have been removed tend to be characterised by reduced diversity of foxes with young sheep at risk (Jones et al., 2003), and thus their reintro- small vertebrates and shifts in vegetation composition (Letnic et al., duction is likely to obtain more support from livestock producers than 2012; Ripple et al., 2014), but these trends are not evidenced in all would the maintenance of dingo populations. Since the turn of the cases (Letnic et al., 2012). 21st century, devils have undergone massive population decline due to Australia's largest mammalian carnivore is the dingo (Canis dingo). an epidemic of devil facial tumour disease (DFTD) (Hollings et al., Dingoes arrived on mainland Australia 5000–3500 years before present 2014). Thus, a mainland population of DFTD-free devils would also func- (ybp) (Letnic et al., 2014). Around the time that the dingo arrived tion as an insurance population in the event that the Tasmanian popula- on mainland Australia, two marsupial predators, the Tasmanian tiger tion became extinct as a result of DFTD or another threatening process. It (Thylacinus cynocephalus) and Tasmanian devil (hereon in devil) is conceivable also, that a reintroduction of devils to the mainland may (Sarcophilus harrisii) became extinct from mainland Australia but succeed because two of the purported drivers of devil decline from the persisted on the island of Tasmania which dingoes never colonised mainland during the Holocene, dingoes and hunting by Aboriginal peo- (Letnic et al., 2014). The coincidence in the timing of the arrival of the ple, are now diminished across much of the mainland and thus may not dingo and extinction of the Tasmanian tiger and devil, coupled with the pose a threat to reintroduced devil populations. fact that larger dingoes were likely to be superior competitors in one We use two approaches to evaluate the potential to reintroduce on one agonistic interactions lends support to the idea that dingoes likely devils to south-eastern Australia. Because devils are now restricted to contributed to the extinction of these marsupial predators from main- the island of Tasmania which has a temperate climate, it is possible land Australia (Letnic et al., 2012). This hypothesis is supported by obser- that extant devils may be poorly adapted to the warmer environments vations that devils are easily killed by domestic dogs (Jones et al., 2003). of mainland Australia. Given this possibility, it makes sense to initially It has also been proposed that increasing human population densi- reintroduce devils to areas that are climatically similar to Tasmania. ties and or climate, not dingoes were the main driver of the extinction Thus, we used species distribution models (SDMs) to identify areas of the Tasmanian tiger and devil from mainland Australia (Johnson that are climatically suitable for devils based on their existing distribu- and Wroe, 2003). Recent analysis of mitochondrial DNA reveals tion in Tasmania. that drought associated with a severe El Niño Southern Oscillation cli- Our second aim was to use fuzzy cognitive maps (FCMs) to predict matic event from 3000–5000 ybp coincided with the decline of devil the ecological outcomes of predator management scenarios. FCMs populations (Brüniche-Olsen et al., 2014). Extreme drought may have predict the outcomes of interactions among multiple input species pushed devil populations to sufficiently low levels that a “predator (Ramsey and Norbury, 2009; Dexter et al., 2012) and are a risk-free, pit” (Sinclair et al., 1998) ensued whereby predation by humans and low input method of testing novel management scenarios. The scenarios dingoes prevented the recovery of devil populations. we investigated involved reintroducing devils in the absence of dingoes Because they kill livestock, dingoes are widely perceived as a pest and and reintroducing devils with dingoes present. We also modelled their populations are controlled in many parts of Australia using poi- presently existing scenarios such as intensive dingo and fox baiting to soned meat baits, trapping and shooting (Allen et al., 2015). However, use as comparative scenarios. there is evidence also that dingoes are a strongly interactive apex predator and that suppression of dingo populations by humans can drive shifts 2. Methods in the abundances of other species (Letnic et al., 2012). Sustained efforts to eradicate dingoes have resulted in irruptions of herbivores such as 2.1. Reintroduction viability using species distribution models (SDMs) kangaroos and wallabies (macropods) (Robertshaw and Harden, 1986; Colman et al., 2014; Allen, 2015) and have, in some but not all cases, We used SDM to determine if climatic conditions are favourable for been linked to increases in the abundance of invasive mesopredators, devil reintroduction to the south-eastern Australian mainland. We used the red fox (Vulpes vulpes) and feral cat (Felis catus)(Gordon et al., 1469 presence records for S. harrisii in Tasmania sourced from the Atlas 2015; Allen et al., 2015; Colman et al., 2014; Johnson and VanDerWal, of Living Australia (Accessed 10 August 2013). 2009; Letnic et al., 2011). In turn, predation by foxes and depletion of Current climate data was sourced from the WorldClim website understorey vegetation by macropods have been identified as drivers which is free to access (www.worldclim.org). Current data ranges for of population decline in small and medium sized mammals in forest WorldClim layers span from the years 1950 to 2000 and are based on ecosystems (Robley et al., 2014; Colman et al., 2014; Foster et al., 2014). Bureau of Meteorology (BOM) records. We used Maxent (Maxent ver. Here we explore the feasibility of reintroducing devils to forest eco- 3.3.1) to generate an output of suitable devil locations on the mainland. systems in south-eastern Australia in order to stem the changes to eco- Outputs were restricted to the Australian mainland as it is the focus system structure associated with lethal control of dingoes. Because area of this study (Fig. 1). We used recent climate scenarios only dingoes are a major pest to livestock producers the maintenance (1950–2000) to determine suitable areas of devil reintroduction. of dingo populations is an untenable option for wildlife managers We initially ran the model with all 19 bioclimatic variables and we in many regions of south-eastern Australia. However, another option then evaluated the output to determine which layers contributed available to wildlife managers may be to fill the apex predator niche most to the model. Bioclimatic variable number 1 (mean annual tem- with the devil. While devils, owing to their smaller body size and slower perature) contributed strongly to the model. We then ran variable 1 metabolism, are unlikely to occupy exactly the same niche as the dingo, with a combination of other variable layers and found number 1 best theory and evidence from Tasmania where they remain extant suggests served our purpose on its own. that devils have similar positive effects on small and medium sized The fit of our model was evaluated using the AUC (area under curve), mammal species as dingoes do (Hollings et al., 2014). This is because where the closer the value is to 1 the better the fit. A value of 0.5 indi- devils can have suppressive effects on the populations and activity pat- cates a model fit no better than random (Elith et al., 2006). terns of native herbivores and invasive mesopredators (Hollings et al., 2014; Jones et al., 2007; Fancourt et al., 2015). Indeed, top down effects 2.2. The fuzzy cognitive model (FCM) of devils has been mooted as one of the reasons why red foxes have not flourished in Tasmania despite several introductions (Jones et al., 2007). Quantitative information about a species' ecology or natural history In addition, the failure of foxes to establish is Tasmania is thought to be is often unknown. Nevertheless, scientists may know whether the effect 430 D.O. Hunter et al. / Biological Conservation 191 (2015) 428–435

Fig. 1. a. Species distribution model of potential Tasmanian devil (Sarcophilus harrisii) distribution on the mainland under the current climate scenario; b. distribution of the dingo (Canis dingo)andhybrids(Canis dingo × Canis familiaris) in Australia. Modified from Letnic et al. (2011). of one species on another is strong, moderate or weak, and whether it is activation function f, used to limit the relative population numbers to a positive or negative effect. Although not numerically precise, this in- the interval [0,1], (Dexter et al., 2012) suggest using a logistic function. formation can be harnessed to produce meaningful ecological informa- We chose a logistic function that approximates the identity function tion for land managers (Ramsey and Veltman, 2005). When used in on the interval [0,1], namely the function below which is illustrated conjunction with fuzzy cognitive models (FCM), this type of data can in Fig. 2: provide powerful qualitative modelling of ecological systems that are 1 highly complex or where data are uncertain (Dambacher et al., 2003). fxðÞ¼ : −4ðÞx−1 Our particular model is a FCM implemented stochastically as a fuzzy 1 þ e 2 Markov-type chain. FCMs represent concepts and their pair-wise interactions as the nodes and edges of mathematical graphs (Kosko, 1986). For each of the 5 scenarios, we calculated a sequence of 1000 itera- In our study, the nodes are species and edges represent interaction tions 100 times and found the 1000 iteration values, averaged over strengths between −1 and 1. These strengths can occasionally be deter- the 100 runs following Dexter et al. (2012). However, we found that mined with high precision but are more often mapped fuzzily by the this was not required in our study. linguistic estimates “very weak”, “weak”, “moderate”,and“high” to the numeric strengths 0.1, 0.2, 0.5, and 0.8, respectively. The graph 2.3. The agents (species and vegetation) can be represented by a matrix E in which each entry eij indicates the interaction strength that species j has on species i. Blank spaces are inter- The SDM identified suitable habitats for devils exist in south-eastern action strengths that we have not been able to determine. In the model, Australia (Fig. 1). The areas identified in the models consists primarily of these spaces are set to 0, with small stochastic perturbations applied at forest habitats dominated by Eucalyptus spp. (Keith, 2004) and lands each step. As demonstrated in Ramsey and Veltman (2005) and further that have been cleared for agricultural purposes. Because the most suit- developed in Ramsey and Norbury (2009) and Dexter et al. (2012), this able habitats for devils existed in forested regions, we calculated inter- matrix representation can be used to add predictive power to the FCM. action strength for our FCMs using data from published studies that We further refined our model, making it more precise, by allowing each have been conducted in this region. entry to assume a set of values such as a single value or an interval of The agents chosen for modelling in this study include species that values, depending on the data available. were likely to be strongly influenced by devil reintroduction and fox Representing the species population distribution as a vector s_i at and dingo predation. To improve the quality of the model we set an ini- time step i, normalised relatively to the interval [0,1] with each species tial abundance value for every agent (Appendix A). population represented by their percentage of the sum of populations, it Initial abundances of agents were calculated using data from a study is simple to calculate the relative population distribution si +1at time reporting the effects of dingo control on forested ecosystems (Colman step i + 1 as a Markov chain process. As in the studies cited above, our study contains inherent uncertainties and these are represented in the model as randomising effects to be applied at each iteration. For these effects, we extended the lower and upper bounds of each interaction strength interval eij by 0.1. At each iteration, an element of this interval is chosen at random to represent eij,and performing this randomisation to each matrix entry gives a randomised effect matrix R(E). Our iteration is then given explicitly as si +1= λf(R(E)si)+(1− λ)si where λ is a relaxation parameter to speed up the asymptotic convergence of the population distributions. As the Fig. 2. The activation function f. D.O. Hunter et al. / Biological Conservation 191 (2015) 428–435 431 et al., 2014) by multiplying interaction strengths by abundance data. occurrence of small mammal in devil diet (b1%) to a correlation (r) Abundance was standardised to a per kilometre metric. value of 0,−0.1 (Jones and Barmuta, 1998). We grouped all palatable vegetation below waist height as “vegeta- All intraspecific interactions were set at 0.1 which assumes that all tion complexity” for our analysis. Multiple small dasyurid species were conspecifics have a slightly positive effect on one another at normal frequently captured (e.g. Antechinus flavipes and Antechinus stuartii)and population densities based on the notion that conspecifics are required because of their similarity we have grouped these as ‘Antechinus’. Simi- for reproduction. larly, red-necked wallaby (Macropus rufogriseus) and swamp wallaby (Wallabia bicolor)aregroupedas‘wallaby’. We included two bandicoot speciesinthisstudy,southernbrownbandicoot(Isoodon obesulus)and 2.5. Model scenarios long-nosed bandicoot (Perameles nasuta), and these have been grouped as ‘bandicoot’. 2.5.1. Baseline scenario — No dingo control, no fox control This scenario is the null scenario against which the effects of all other scenarios were compared (Fig. 3). It represents areas of National Parks 2.4. Data extraction that do not conduct any dingo baiting and we assume dingoes exist at ecologically effective densities. We modelled this scenario by not cap- Most of the interaction strengths we used to populate our FCM were ping the abundance of any species and allowing them to ‘naturally’ gleaned from the literature using a meta-analytic approach comparing interact. the effects of predation on other species in the forested ecosystems of south-eastern Australia (Appendix B). Raw data was used to extract t or f values if they were not readily available. All interaction values 2.5.2. Scenario 2 — Complete dingo eradication and complete fox were then converted to product moment correlation (r)valuesin eradication MetaWin (http://www.metawinsoft.com). Each r value represents the This scenario simulates intensive control of both dingoes and foxes interaction strength between a pair of agents (Table 1). For instances such that their populations are below densities at which they are eco- where published data was scant or absent between a pair of agents logically effective (sensu Soule et al., 2003). In a field situation this we inferred interaction strengths using the literature or expert opinion would be achieved for dingoes by targeted leg hold trapping and baiting (Appendix B). with 1080 (sodium fluoroacetate) dosed meat baits. Nominal dose for Where information was especially scant for the effect of devil on dingoes is 6 mg of pure 1080 per bait (Fleming and Parker, 1991). Inten- bush rat (Rattus fuscipes)andAntechinus spp. we used published infor- sive fox control is achieved with 1080 meat baiting, nominal dose 3 mg mation on the diet of devils to infer weak interaction strengths based of 1080 per bait (Claridge et al., 2010; Marks and Wilson, 2005). In the on the notion that predation on these species may have negative effects model we simulate this scenario by holding dingo and fox abundance on their populations (Appendix B4). We converted the frequency of at 0.

Table 1 Interaction matrix populated with interaction strengths (r). To be read as effect of column on row.

Wallaby Rock wallaby Kangaroo B/tail possum R/tail possum Wombat Greater glider Quoll Bandicoot

Wallaby 0.10 −0.10 −0.20 −0.10 (−0.1, 0.2) Rock wallaby −0.10 0.10 −0.10 −0.10 −0.10 Kangaroo −0.10 −0.10 0.10 −0.10 B/tail possum 0.10 −0.20 −0.80 R/tail possum −0.20 0.10 −0.80 Wombat −0.10 −0.10 −0.10 0.10 Greater glider −0.50 −0.20 0.10 −0.80 Quoll 0.10 0.10 (0.2,0.5) 0.20 0.80 0.10 (0.2,0.5) Bandicoot −0.10 −0.10 −0.10 −0.10 −0.50 0.10 Bush rat −0.10 −0.20 Antechinus spp. −0.10 −0.20 Cat 0.10 0.20 0.10 0.80 −0.50 0.20 Fox 0.80 0.50 0.20 0.50 0.10 0.10 0.10 −0.20 0.50 Dingo 0.50 0.20 0.50 0.20 0.10 0.50 0.10 Devil 0.50 0.50 0.20 0.20 0.20 0.20 0.10 −0.30 0.10 Vegetation complexity −0.20 −0.20 −0.20 −0.10 −0.10 −0.10 −0.10

Bush rat Antechinus spp. Cat Fox Dingo Devil Vegetation complexity

Wallaby −0.20 −0.30 −0.71 −0.52 0.80 Rock wallaby −0.20 −0.97 −0.20 −0.52 0.80 Kangaroo −0.28 −0.43 −0.52 0.10 B/tail possum −0.50 −0.70 −0.21 −0.31 0.50 R/tail possum −0.50 −0.48 −0.21 0.14 0.80 Wombat 0.13 0.17 −0.80 0.10 Greater glider −0.50 −0.10 −0.21 0.14 0.50 Quoll (0, 0.2) 0.20 −0.50 0.20 −0.10 Bandicoot −0.80 −0.34 0.42 0.14 0.60 Bush rat 0.10 −0.80 0.39 0.66 (0,0.10) 0.80 Antechinus spp. 0.10 −0.80 −0.35 0.62 (0,0.10) 0.40 Cat 0.50 0.20 0.10 0.06 −0.26 −0.58 Fox 0.50 0.10 −0.10 0.10 −0.25 −0.60 Dingo (0.1,0.2) −0.10 0.10 −0.10 Devil 0.1 −0.10 −0.20 −0.60 0.10 Vegetation complexity 0.19 0.20 0.10 432 D.O. Hunter et al. / Biological Conservation 191 (2015) 428–435

Fig. 3. Percentage shifts in abundance, expressed as the proportional change, for each agent under all scenarios. More extreme shifts are equivalent to strong cascading effects. Dark grey bars represent the initial capped abundance value. Black bars represent Tasmanian devil abundance.

2.5.3. Scenario 3 — No dingo or fox control, devil reintroduced control activities. It is the same as scenario 4 but with no cap on devil This scenario simulates introducing devils into ecosystems where abundance. We've assumed minimal unintended devil fatalities as a re- neither dingoes or foxes are controlled and assumes that devils can sult of dingo baiting since devils are 38 times more resistant to 1080 co-exist with dingoes. In the model we achieved this scenario by not than dingoes (Mcilroy, 1981). Additionally, burying baits to 15 cm re- capping dingo or fox abundance and by adding devils to the model. duces the likelihood of devils removing baits (Hughes et al., 2011).

3. Results 2.5.4. Scenario 4 — Complete dingo eradication, reduced fox abundance This scenario simulates control activities directed towards dingoes 3.1. Habitat suitability of devils on mainland Australia but not foxes. Such situations can arise when dingo control programmes are undertaken with the purpose of protecting livestock but foxes are The final SDM AUC value was 0.927, representing a good fit. The not targeted. Under this scenario dingo control is intensive as outlined model indicates that under current conditions habitats of high suitabil- in scenario 2, however, some fox mortality is expected to occur as a re- ity occur mainly in south-eastern Australia (Fig. 1). Many areas where sult of foxes consuming baits laid for dingoes (Fleming and Parker, devils are climatically suited coincide with areas where dingoes are 1991). To create this scenario in the FCM we limited dingo abundance rare or absent (Fig. 1b). to 0 and fox abundance to 50% of unbaited levels. 3.2. FCM model 2.5.5. Scenario 5 — Complete dingo eradication, reduced fox abundance and devil reintroduced The convergence of each thousand-value set was rapid and stable, This scenario explores the effects of introducing devils to areas even for high values of λ, with the maximal average absolute difference where dingoes have been removed and some foxes are killed by dingo between two of any sequential species populations being less than 0.8%, D.O. Hunter et al. / Biological Conservation 191 (2015) 428–435 433 and most differences being far smaller. This convergence and stability 4. Discussion was due to the high ratio of matrix entries in E that we determined. Our SDM suggests that it would be feasible to reintroduce devils to the forests of south-eastern Australia and establish a disease-free “in- 3.3. FCM scenarios surance” population because climatically suitable areas exist there (Fig. 1). FCM modelling suggests that once established, devils could as- 3.3.1. Scenario 2 — Complete dingo eradication and complete fox eradication sume a similar ecological role to dingoes in places where dingoes have The predicted effect of removing dingoes reduced vegetation com- been eradicated (Fig. 1) by suppressing the abundances of invasive plexity by 25% while wallaby numbers grew 95% (see Table 2 for species mesopredators and wallabies (Fig. 4). response values). Antechinus and bush rat numbers fell 31% and 34% re- A scenario that we did not consider in our FCM exercise was that spectively. Brush-tailed rock wallaby (Petrogale penicillata) numbers devils may be pre-adapted to the climate of mainland Australia. Such a increased (119%) while Spotted-tailed quolls (Dasyurus maculatus) scenario is not unrealistic because devils were found throughout main- (hereon in quolls) also increased markedly (68%). Macropod species land Australia during the Holocene and only became extinct less than benefited the most under this scenario (Table 2, Fig. 4). 3000 years ago (Letnic et al., 2014). Further research could use mechanistic models to identify areas on the mainland where devils could 3.3.2. Scenario 3 — No dingo or fox control, devil reintroduced thrive (Kearney et al., 2010). If devils are pre-adapted to the mainland This scenario exhibited an overall reduction of extreme cascades climate, we would expect them to have little difficulty becoming evident in the model output by low shifts in the abundance of the established in the areas of south-eastern and south-western Australia model agents (Table 2, Fig. 4). Cat and fox abundance decreased in the where dingoes have been eradicated and hunting of native mammal presence of the devil by 13% and 14% respectively (Table 2, Fig. 4). species by humans is highly regulated. However, if dingoes were the Greater gliders (Petauroides volans), bandicoots and ringtail possums cause of devil extinction from mainland Australia, devils may be unlike- (Pseudocheirus peregrinus) all increased by at least 10% (Table 2, ly to establish populations in regions where dingo populations remain Fig. 4). Rock wallabies and wallabies showed only negligible decreases (Letnic et al., 2012). If a formal devil introduction was to be undertaken, (1–4%). Vegetation complexity benefits most under this scenario likely a reintroduction strategy would need to consider ways to minimize po- attributed to lower abundances of medium and large herbivores. tential competitive effects of canids on reintroduced devils, particularly for founding populations of devils. Testament to the strength of our FCM is its accurate emulation 3.3.3. Scenario 4 — Complete dingo eradication, reduced fox abundance of empirical field observations for the currently existing and testable Removing dingoes resulted in population growth of most macropod scenarios 2 and 4. In accord with field observations, our model demon- species (Table 2, Fig. 4). Despite applying a 50% constraint on fox strates that cascading effects ensue once dingoes are completely eradi- growth, numbers increase markedly in this scenario (Table 2, Fig. 4). cated. Notably, foxes became more common as expected under the Cat abundance increases 5% (Table 2, Fig. 4). All terrestrial small and MRH (Brook et al., 2012; Johnson and VanDerWal, 2009). In accord medium sized mammal species experience negative growth. with trophic cascade theory and field studies, complete eradication of dingoes and foxes was associated with increased abundance of 3.3.4. Scenario 5 — Complete dingo eradication, reduced fox abundance and macropods and a reduction in vegetation complexity (Colman et al., devil reintroduced 2014; Dexter et al., 2013). Macropods mostly respond positively to this scenario (Table 2, In our modelling the complete eradication of dingoes and foxes in- Fig. 4). Cats declined 14% compared to the same scenario without devils. creased abundances of threatened species, the spotted-tailed quoll Fox abundance almost halved compared to the same scenario without and rock wallaby, which is consistent with field studies reporting the ef- devils. Bandicoot, ringtail possum, Antechinus, bush rat and greater glid- fects of fox baiting on rock wallabies (Kinnear et al., 1988). Although er abundances increased compared to the same scenario without devils canid baiting is the status quo management option for threatened spe- (Table 2, Fig. 4). cies management in much of south-eastern Australia, our modelling suggests that canid eradication can result in the decline of some native mammal species. In our FCM canid eradication resulted in decreased Table 2 Output values from FCM displayed here as percentage shift from null state (scenario 1). abundances of small and medium sized mammals such as bush rats, Antechinus spp. and bandicoots due to increased impacts of introduced Predator Scenario Scenario 1 Scenario 2 Scenario 3 Scenario 4 Scenario 5 mesopredators and macropods. However, we caution, that although Baited dingo ✓✓✓our models do suggest shifts in mammal abundances consistent with Baited fox ✓ theory and previous field studies, a shortcoming of our FCM is that not Reduced fox ✓✓ all strengths of interactions are known and predictions are limited to Tasmanian devil ✓✓ the species included in our models. Model agents One way to restore top-down control of herbivores and introduced

Veg. complexity 0% −25% +7% −18% −6% mesopredators in areas where dingoes have been extirpated may be Kangaroo 0% +73% −10% +38% +13% by reintroducing devils (Ritchie et al., 2012). Under scenario 5 where Wombat 0% −27% −25% −15% −46% we simulated the reintroduction of devils under the assumption that Wallaby 0% +95% −4% +64% +43% dingoes and devils could not coexist, the abundances of red foxes, Rock wallaby 0% +119% −1% −1% 0% macropods and wombats (Vombatus ursinus) decreased. Conversely, Fox 0% −100% −14% +124% +68% Cat 0% 0% −13% +5% −19% the abundances of Antechinus, ringtail possums, bandicoots, greater Brushtail possum 0% +56% 0% +4% +6% gliders, brushtail possums (Trichosurus vulpecula) and vegetation com- Spotted-tailed quoll 0% +68% +9% +5% +19% plexity all increased relative to the same scenario without devils. Greater glider 0% −9% +10% +10% +26% ﬁ − − − Our results suggest that devils can ful l a similar ecological function Bandicoot 0% 31% +15% 39% 18% ﬁ Ringtail possum 0% +23% +17% +3% +33% to dingoes and are consistent with eld studies from Tasmania where Bush rat 0% −34% +10% −50% −35% devils have been reported to suppress the abundances of feral cats and Antechinus 0% −31% +8% −47% −33% small macropods (Hollings et al., 2014; but see also Fancourt et al., Dingo 0% −100% −9% −100% −100% 2015). However, devils' overall effects on ecosystems are expected to Tasmanian devil 0% 0% +62% 0% +100% be weaker than those of dingoes due to their smaller body size and 434 D.O. Hunter et al. / Biological Conservation 191 (2015) 428–435

Fig. 4. Predicted abundance for agents under each of the 5 scenarios. White bars are the status quo (scenario 1), black bars = dingo and fox eradication (scenario 2), light grey bars = no canid control with devils reintroduced (scenario 3), dark grey bars = dingo eradication (scenario 4) and freckled bars = dingo eradication with devils reintroduced (scenario 5). lower metabolic demands (Letnic et al., 2014). Nonetheless, the failure Parks of south-eastern Australia where the aim of predator control is of red foxes to establish large populations in Tasmania despite similar protecting threatened fauna (Robley et al., 2014; Kovacs et al., 2012) climatic conditions to mainland areas where foxes have thrived in the and controlling dingoes to protect livestock on nearby properties absence of dingoes suggest that there is considerable merit in the idea (Colman et al., 2014), respectively. Unfortunately both of these scenarios of using devils to suppress the abundance and impacts of red foxes are characterised by extremes in species abundances at various trophic (McCallum and Jones, 2006; Jones et al., 2003). However, it is important levels demonstrating poor equitability. The threatened species included to note that the idea that devils suppress foxes is not based on observa- in our simulations, quolls and rock wallabies, both responded positively tions between the two species in the field, but is rather the most plausi- to intensive predator control. However, under this scenario cats and ble hypothesis mooted so far to explain why foxes have not thrived in wallabies increased in abundance and small mammals declined directly Tasmania (Jones et al., 2007; Ritchie et al., 2012). Experiments could as a result of predation from cats but also indirectly, since wallabies de- be conducted to explore devil and fox introductions but would need crease available cover for small mammals (Dexter et al., 2013). to overcome prohibitive ethical, legal and logistic impediments. From a biodiversity conservation perspective scenario 3 benefits Under scenario 3 where we assumed that dingoes and devils can co- many species since dingoes are not eradicated, devils are present in exist, the changes in the abundance of the model agents were not as ex- the ecosystem and foxes and cats are suppressed and there is positive treme as under other scenarios (Fig. 4) which may suggest overall population growth for most small and medium native mammal species cascade strength is dampened with increasing diversity within the and vegetation complexity. Despite positive biodiversity outcomes, sce- predator guild. The importance of maintaining predator diversity nario 3 provides nearby livestock producers with limited protection (Finke and Denno, 2004) and effective population densities of predators from dingo attacks because dingoes remain present. Scenario 5 on the (Soule et al., 2003) in order to mitigate ecological degradation, although other hand sees devils introduced into areas with few canids. The addi- often discussed, has not been thoroughly tested in Australia. One expla- tion of devils is associated with increased abundances of most small and nation for dampening of trophic cascades with increasing predator di- medium mammal species and vegetation complexity increases also versity in our simulations is that more predator diversity increases (Fig. 4). Under scenario 5, the effects of foxes, cats and macropods are competition and predation among guild members and this competition ameliorated without ceasing dingo control. However, the most threat- nullifies their direct effects on prey species (Finke and Denno, 2004). ened species in our simulated system, quolls and rock wallabies, differ little from scenario 1 because these species are in the optimal prey 4.1. An ecological case for reintroducing devils to mainland Australia size range for both foxes and devils (Jones and Barmuta, 2000; Jones, 1997). Scenario 5 may also be desirable to livestock farmers because Our modelling is consistent with results of field studies which sug- dingo spill-over from public to private land is managed. gest that manipulating the abundances of large carnivores can shift Our modelling demonstrates some of the cascading effects of dingo mammal assemblages to alternate states dominated by herbivores and removal may be mitigated by restoring lost predator function with mesopredators (Estes et al., 2011; Ripple et al., 2014). Which of these devils. Scenarios with devils tended to have the most equitable assem- states is most desirable is subjective. For example, scenarios 2 and 4 rep- blages exhibiting less extreme cascades. However, introducing devils resent predator management regimes undertaken in some National to the system provided little benefit for the most threatened mammal D.O. Hunter et al. / Biological Conservation 191 (2015) 428–435 435 species, because devils also predate on many of these species (Jones and Johnson, C., 2006. Australia's Mammal Extinctions: a 50 000 Year History. Cambridge University Press. Barmuta, 2000; Jones, 1997). Hence from a management perspective, Johnson, C.N., VanDerWal, J., 2009. Evidence that dingoes limit abundance of a devil introduction appears likely to provide considerable benefits for mesopredator in eastern Australian forests. J. Appl. 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