Influence of interactive effects on long-term population trajectories in multispecies reintroductions.

Reintroduced populations are typically considered to progress through establishment, growth, and regulatory phases. However, most reintroduction programs do not monitor intensively enough to test this conceptual model. We studied population indices derived from track activity of 4 threatened species (greater bilby [Macrotis lagotis], burrowing bettong [Bettongia lesueur], greater stick-nest rat [Leporillus conditor], and Shark Bay bandicoot [Perameles bougainville]) over 23 years after multiple reintroductions of each species in arid Australia. We compared population trajectories among species and investigated the effect of time and environmental variables. All species bred immediately after release, and the growth phase lasted 3-16 years, varying markedly among but not within species. The end of the growth phase was characterized by an obvious peak in population density followed by either a catastrophic decline and sustained low density (bettongs), a slow decline to extirpation after 20 years (stick-nest rat), or a slight decline followed by irregular fluctuations (bilby and bandicoot). Minor fluctuations were related to environmental variables, including 12-month cumulative rainfall and lagged summer maximum temperatures. Three of the 4 species did not reach a regulation phase, even after 23 years, possibly due to interspecific competition and trophic cascades triggered by predator removal and multispecies reintroductions. Bilbies and bandicoots exhibited a second growth phase 18 years after reintroduction, likely caused by high rainfall and increased resources following the population crash of overabundant bettongs. Our results suggest that assemblages within multispecies reintroductions demonstrate high variability in population trajectories due to interactive effects. Intensive monitoring to assess population viability may require decades, particularly where multiple species are reintroduced, release sites are confined, and the climate is unpredictable. Intensive monitoring also allows for adaptive management to prevent precipitous population declines. Practitioners should not assume reintroduced species pass through predictable postrelease population phases or that viability is assured after a certain period.

Influencia de los efectos interactivos sobre la trayectoria a largo plazo de las poblaciones en reintroducciones de múltiples especies Resumen Comúnmente se considera que las poblaciones reintroducidas progresan cuando se establecen, crecen y atraviesan fases regulatorias. Sin embargo, casi todos los programas de reintroducción no monitorean lo suficiente para evaluar este modelo conceptual. Estudiamos los índices poblacionales derivados de la actividad de rastreo de cuatro especies amenazadas (Macrotis lagotis, Bettongia lesueur, Leporillus conditor, y Perameles bougainville) más de 23 años después de varias reintroducciones de cada especie en las zonas áridas de Australia. Comparamos las trayectorias poblacionales entre especies e investigamos el efecto del tiempo y las variables ambientales. Todas las especies se reprodujeron inmediatamente después de la liberación, y la fase de crecimiento duró entre 3 y 16 años, con una variación marcada entre, pero no dentro de las especies. El final de la fase de crecimiento se caracterizó por un pico obvio en la densidad poblacional seguido de una declinación catastrófica o una baja densidad sostenida (B. lesueur), una declinación lenta ante la extirpación 20 años después (L. conditor) o una declinación leve seguida de fluctuaciones irregulares (M. lagotis y P. bougainville). Las fluctuaciones menores estuvieron relacionadas con las variables ambientales, incluyendo la precipitación acumulada de 12 meses y el retraso en las temperaturas máximas de verano. Tres de las cuatro especies no llegaron a la fase regulatoria, incluso después de 23 años, posiblemente por la competencia interespecífica y las cascadas tróficas causadas por la eliminación de depredadores y la reintroducción de varias especies. M. lagotis y P. bougainville exhibieron una segunda fase de crecimiento 18 años después de la reintroducción, probablemente causada por la precipitación elevada y el incremento de recursos después de la crisis poblacional por sobreabundancia de B. lesueur. Nuestros resultados sugieren que los conjuntos dentro de la reintroducción de múltiples especies demuestran una gran variabilidad en las trayectorias poblacionales debido a los efectos interactivos. El monitoreo intenso para evaluar la viabilidad poblacional puede llevar varias décadas, particularmente cuando se reintroducen varias especies, en donde los sitios de liberación están confinados y en donde el clima es impredecible. El monitoreo intensivo también permite que el manejo adaptativo prevenga una declinación poblacional precipitada. Quienes practican la conservación no deberían asumir que una especie reintroducida atraviesa fases predecibles después de la liberación o que la viabilidad está asegurada después de cierto periodo.

Long-Distance Movements of Feral Cats in Semi-Arid South Australia and Implications for Conservation Management.

Movements that extend beyond the usual space use of an animal have been documented in a range of species and are particularly prevalent in arid areas. We present long-distance movement data on five feral cats (Felis catus) GPS/VHF-collared during two different research projects in arid and semi-arid Australia. We compare these movements with data from other feral cat studies. Over a study period of three months in the Ikara-Flinders Ranges National Park, 4 out of 19 collared cats moved to sites that were 31, 41, 53 and 86 km away. Three of the cats were males, one female; their weight was between 2.1 and 4.1 kg. Two of the cats returned to the area of capture after three and six weeks. During the other study at Arid Recovery, one collared male cat (2.5 kg) was relocated after two years at a distance of 369 km from the area of collar deployment to the relocation area. The movements occurred following three years of record low rainfall. Our results build on the knowledge base of long-distance movements of feral cats reported at arid study sites and support the assertion that landscape-scale cat control programs in arid and semi-arid areas need to be of a sufficiently large scale to avoid rapid reinvasion and to effectively reduce cat density. Locally, cat control strategies need to be adjusted to improve coverage of areas highly used by cats to increase the efficiency of control operations.

Genomic Approaches for Conservation Management in Australia under Climate Change.

Conservation genetics has informed threatened species management for several decades. With the advent of advanced DNA sequencing technologies in recent years, it is now possible to monitor and manage threatened populations with even greater precision. Climate change presents a number of threats and challenges, but new genomics data and analytical approaches provide opportunities to identify critical evolutionary processes of relevance to genetic management under climate change. Here, we discuss the applications of such approaches for threatened species management in Australia in the context of climate change, identifying methods of facilitating viability and resilience in the face of extreme environmental stress. Using genomic approaches, conservation management practices such as translocation, targeted gene flow, and gene-editing can now be performed with the express intention of facilitating adaptation to current and projected climate change scenarios in vulnerable species, thus reducing extinction risk and ensuring the protection of our unique biodiversity for future generations. We discuss the current barriers to implementing conservation genomic projects and the efforts being made to overcome them, including communication between researchers and managers to improve the relevance and applicability of genomic studies. We present novel approaches for facilitating adaptive capacity and accelerating natural selection in species to encourage resilience in the face of climate change.

Exploring the internal and external wildlife gradients created by conservation fences.

Spillover effects are an expansion of conservation benefits beyond protected areas through dispersal of species that reside within. They have been well documented in marine but not terrestrial systems. To understand the effects on wildlife created by conservation fences, we explored the internal and external gradients of activity in mammal, reptile, and bird species at a conservation reserve in arid Australia that is fenced to exclude invasive rabbits (Oryctolagus cuniculus), cats (Felis catus), and foxes (Vulpes vulpes). Two methods were used: counts of animal tracks along transects on sand dunes and captures at pitfall-trapping sites. In both cases, sites were spaced at different distances from the reserve fenceline inside and outside the reserve. We recorded a range of spillover, source-sink, step, and barrier effects that combined to create a zone within and around the reserve with fence-induced species-specific wildlife gradients. Two endemic rodents but none of the 4 mammal species reintroduced to the reserve showed positive spillover effects. Barrier effects, where activity was highest close to the fence, were recorded for the feral cat and native bettong (Bettongia lesueur), species that could not breach the fence. In comparison, some reptiles and native mammal species that could permeate the fence displayed source-sink effects; that is, their activity levels were reduced close to the fence likely due to constant emigration to the side with lower density. Activity of some reptiles was lowest at sites inside the reserve and gradually increased at outside sites with distance from the fence, a gradient likely related to trophic cascades triggered by predator exclusion. Our result shows that fenced reserves can create overlapping layers of species-specific gradients related to each species' ability to permeate the fence and its varying susceptibility to threats. Managers should be aware that these gradients may extend for several kilometers either side of the fence and that not all contained species will increase in abundance. Creating wider conservation benefits may require increased fence permeability and threat reduction outside the fence.

Exploración de los gradientes de vida silvestre internos y externos creados por las vallas de conservación. Resumen Los efectos de derrame son una expansión de los beneficios de conservación más allá de las áreas protegidas a través de la dispersión de especies que residen en su interior. Han sido bien documentados en sistemas marinos, pero no terrestres. Para entender los efectos de las vallas de exclusión sobre la vida silvestre, exploramos los gradientes internos y externos de la actividad de especies de mamíferos, reptiles y aves en una reserva de conservación en la región árida de Australia que está cercada para excluir conejos invasivos (Oryctolagus cuniculus), gatos (Felis catus) y zorros (Vulpes vulpes). Se utilizaron dos métodos: conteo de huellas de animales a lo largo de transectos en dunas de arena y captura con trampas pitfall. En ambos casos, los sitios fueron espaciados a distintas distancias dentro y fuera de la valla de la reserva. Registramos una gama de efectos de derrame, fuente-sumidero, escalón y barrera que se combinaron para crear una zona dentro y alrededor de la reserva con gradientes de vida silvestre inducidos por la valla. Dos roedores endémicos, pero ninguna de 4 especies de mamíferos reintroducidas a la reserva, mostraron efectos de derrame positivos. Los efectos de barrera, donde la actividad era mayor cerca de la valla, fueron registrados para el gato feral y la rata canguro nativa (Bettongia lesueur), especies que no pudieron franquear la valla. En contraste, algunas especies de reptiles y mamíferos nativos que pudieron permear la valla mostraron efectos de fuente-sumidero; esto es, sus niveles de actividad fueron bajos cerca de la valla probablemente debido a la emigración constante hacia el lado con menor densidad. La actividad de algunos reptiles fue menor en los sitios núcleo de la reserva e incrementaron a medida que incrementó la distancia hacia afuera, un gradiente relacionado probablemente con las cascadas tróficas desencadenadas por la exclusión de depredadores. Nuestros resultados muestran que las reservas cercadas pueden crear capas sobrepuestas de gradientes específicos relacionados con la habilidad de cada especie para permear la valla y su susceptibilidad a las amenazas. Los manejadores deber ser conscientes de que esos gradientes pueden extenderse varios kilómetros a ambos lados de la valla y que no todas las especies contenidas aumentarán en abundancia. La creación de beneficios de conservación más amplios puede requerir una mayor permeabilidad de la vallas y la reducción de amenazas fuera de la reserva.

Taxonomic status of the Australian dingo: the case for Canis dingo Meyer, 1793.

The taxonomic status and systematic nomenclature of the Australian dingo remain contentious, resulting in decades of inconsistent applications in the scientific literature and in policy. Prompted by a recent publication calling for dingoes to be considered taxonomically as domestic dogs (Jackson et al. 2017, Zootaxa 4317, 201-224), we review the issues of the taxonomy applied to canids, and summarise the main differences between dingoes and other canids. We conclude that (1) the Australian dingo is a geographically isolated (allopatric) species from all other Canis, and is genetically, phenotypically, ecologically, and behaviourally distinct; and (2) the dingo appears largely devoid of many of the signs of domestication, including surviving largely as a wild animal in Australia for millennia. The case of defining dingo taxonomy provides a quintessential example of the disagreements between species concepts (e.g., biological, phylogenetic, ecological, morphological). Applying the biological species concept sensu stricto to the dingo as suggested by Jackson et al. (2017) and consistently across the Canidae would lead to an aggregation of all Canis populations, implying for example that dogs and wolves are the same species. Such an aggregation would have substantial implications for taxonomic clarity, biological research, and wildlife conservation. Any changes to the current nomen of the dingo (currently Canis dingo Meyer, 1793), must therefore offer a strong, evidence-based argument in favour of it being recognised as a subspecies of Canis lupus Linnaeus, 1758, or as Canis familiaris Linnaeus, 1758, and a successful application to the International Commission for Zoological Nomenclature - neither of which can be adequately supported. Although there are many species concepts, the sum of the evidence presented in this paper affirms the classification of the dingo as a distinct taxon, namely Canis dingo.

Non-invasive monitoring of adrenocortical physiology in a threatened Australian marsupial, the western quoll (Dasyurus geoffroii).

Reintroduction has become an increasingly important conservation tool in Australia, yet the effects of stress on species during reintroduction programs have received little attention. The use of enzyme immunoassays to measure faecal glucocorticoid metabolites (FGM) is a useful non-invasive technique to monitor adrenal activity but requires validation before they can be reliably used. As part of a large reintroduction project, the goals of this study were to 1) monitor FGM in 53 western quolls (Dasyurus geoffroii) following capture from the wild and transfer to a holding facility and use this stressor to biologically validate an enzyme immunoassay; 2) determine if biological factors, such as sex, age, weight or source population affect baseline FGM levels; and 3) examine individual variation in the acute adrenal response of quolls to the capture and transfer associated with reintroductions. We successfully validated an assay that targets glucocorticoid metabolites with a 5α-3ß,11ß-diol structure and found that sex significantly influenced both baseline and peak FGM output in western quolls, whereas age, weight and source population did not. We also observed considerable variation among individuals in the magnitude and duration of their physiological response to capture and transfer. Using the methods described here, FGM analysis may provide further information about the adrenal activity of the western quoll and improve future conservation efforts for this threatened species.

In situ predator conditioning of naive prey prior to reintroduction.

Many translocations and introductions to recover threatened populations fail because predators kill prey soon after release; a problem exacerbated for predator-naive prey. While pre-release training has been shown to work in some situations, it is time consuming and relies on using inferred predator cues and treating small groups. We review a relatively new and very promising management tool: in situ, pre-release predator conditioning. Here, the goal is to allow prey in large enclosures to live with low densities of predators to accelerate selection for antipredator traits (in an evolutionary sense) or provide prey essential experience with predators that they will later encounter. We review the published results of a large-scale, controlled experiment where we have permitted burrowing bettongs (Bettongia lesueur) and greater bilblies (Macrotis lagotis) to live with low densities of feral cats (Felis catus), a species implicated in their widespread decline and localized extinction. We found that both species could persist with cats, suggesting that future work should define coexistence thresholds-which will require knowledge of prey behaviour as well as the structure of the ecological community. Compared to control populations, predator-naive prey exposed to cats has a suite of morphological and behavioural responses that seemingly have increased their antipredator abilities. Results suggest that predator-conditioned bilbies survive better when released into a large enclosure with an established cat population; future work will determine whether this increased survival extends to the wild. This article is part of the theme issue 'Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation'.

How practitioners integrate decision triggers with existing metrics in conservation monitoring.

Decision triggers are defined thresholds in the status of monitored variables that indicate when to undertake management, and avoid undesirable ecosystem change. Decision triggers are frequently recommended to conservation practitioners as a tool to facilitate evidence-based management practices, but there has been limited attention paid to how practitioners are integrating decision triggers into existing monitoring programs. We sought to understand whether conservation practitioners' use of decision triggers was influenced by the type of variables in their monitoring programs. We investigated this question using a practitioner-focused workshop involving a structured discussion and review of eight monitoring programs. Among our case studies, direct measures of biodiversity (e.g. native species) were more commonly monitored, but less likely to be linked to decision triggers (10% with triggers) than measures being used as surrogates (54% with triggers) for program objectives. This was because decision triggers were associated with management of threatening processes, which were often monitored as a surrogate for a biodiversity asset of interest. By contrast, direct measures of biodiversity were more commonly associated with informal decision processes that led to activities such as management reviews or external consultation. Workshop participants were in favor of including more formalized decision triggers in their programs, but were limited by incomplete ecological knowledge, lack of appropriately skilled staff, funding constraints, and/or uncertainty regarding intervention effectiveness. We recommend that practitioners consider including decision triggers for discussion activities (such as external consultation) in their programs as more than just early warning points for future interventions, particularly for direct measures. Decision triggers for discussions should be recognized as a critical feature of monitoring programs where information and operational limitations inhibit the use of decision triggers for interventions.

The role of refuges in the persistence of Australian dryland mammals.

Irruptive population dynamics are characteristic of a wide range of fauna in the world's arid (dryland) regions. Recent evidence indicates that regional persistence of irruptive species, particularly small mammals, during the extensive dry periods of unpredictable length that occur between resource pulses in drylands occurs as a result of the presence of refuge habitats or refuge patches into which populations contract during dry (bust) periods. These small dry-period populations act as a source of animals when recolonisation of the surrounding habitat occurs during and after subsequent resource pulses (booms). The refuges used by irruptive dryland fauna differ in temporal and spatial scale from the refugia to which species contract in response to changing climate. Refuges of dryland fauna operate over timescales of months and years, whereas refugia operate on timescales of millennia over which evolutionary divergence may occur. Protection and management of refuge patches and refuge habitats should be a priority for the conservation of dryland-dwelling fauna. This urgency is driven by recognition that disturbance to refuges can lead to the extinction of local populations and, if disturbance is widespread, entire species. Despite the apparent significance of dryland refuges for conservation management, these sites remain poorly understood ecologically. Here, we synthesise available information on the refuges of dryland-dwelling fauna, using Australian mammals as a case study to provide focus, and document a research agenda for increasing this knowledge base. We develop a typology of refuges that recognises two main types of refuge: fixed and shifting. We outline a suite of models of fixed refuges on the basis of stability in occupancy between and within successive bust phases of population cycles. To illustrate the breadth of refuge types we provide case studies of refuge use in three species of dryland mammal: plains mouse (Pseudomys australis), central rock-rat (Zyzomys pedunculatus), and spinifex hopping-mouse (Notomys alexis). We suggest that future research should focus on understanding the species-specific nature of refuge use and the spatial ecology of refuges with a focus on connectivity and potential metapopulation dynamics. Assessing refuge quality and understanding the threats to high-quality refuge patches and habitat should also be a priority. To facilitate this understanding we develop a three-step methodology for determining species-specific refuge location and habitat attributes. This review is necessarily focussed on dryland mammals in continental Australia where most refuge-based research has been undertaken. The applicability of the refuge concept and the importance of refuges for dryland fauna conservation elsewhere in the world should be investigated. We predict that refuge-using mammals will be widespread particularly among dryland areas with unpredictable rainfall patterns.

Rabbit biocontrol and landscape-scale recovery of threatened desert mammals.

Funding for species conservation is insufficient to meet the current challenges facing global biodiversity, yet many programs use expensive single-species recovery actions and neglect broader management that addresses threatening processes. Arid Australia has the world's worst modern mammalian extinction record, largely attributable to competition from introduced herbivores, particularly European rabbits (Oryctolagus cuniculus) and predation by feral cats (Felis catus) and foxes (Vulpes vulpes). The biological control agent rabbit hemorrhagic disease virus (RHDV) was introduced to Australia in 1995 and resulted in dramatic, widespread rabbit suppression. We compared the area of occupancy and extent of occurrence of 4 extant species of small mammals before and after RHDV outbreak, relative to rainfall, sampling effort, and rabbit and predator populations. Despite low rainfall during the first 14 years after RHDV, 2 native rodents listed by the International Union for Conservation of Nature (IUCN), the dusky hopping-mouse (Notomys fuscus) and plains mouse (Pseudomys australis), increased their extent of occurrence by 241-365%. A threatened marsupial micropredator, the crest-tailed mulgara (Dasycercus cristicauda), underwent a 70-fold increase in extent of occurrence and a 20-fold increase in area of occupancy. Both bottom-up and top-down trophic effects were attributed to RHDV, namely decreased competition for food resources and declines in rabbit-dependent predators. Based on these sustained increases, these 3 previously threatened species now qualify for threat-category downgrading on the IUCN Red List. These recoveries are on a scale rarely documented in mammals and give impetus to programs aimed at targeted use of RHDV in Australia, rather than simply employing top-down threat-based management of arid ecosystems. Conservation programs that take big-picture approaches to addressing threatening processes over large spatial scales should be prioritized to maximize return from scarce conservation funding. Further, these should be coupled with long-term ecological monitoring, a critical tool in detecting and understanding complex ecosystem change.

Harnessing natural selection to tackle the problem of prey naïveté.

Many populations are threatened or endangered because of excessive predation resulting from individuals' inability to recognize, avoid, or escape alien predators. Such prey naïveté is often attributed to the absence of prior experience and co-evolution between native prey and introduced predators. Many reintroduction programs focus on reducing predation rate by excluding introduced predators, a focus which ignores, and indeed exacerbates, the problem of prey naïveté. We argue for a new paradigm in reintroduction biology that expands the focus from predator control to kick-starting learning and evolutionary processes between alien predators and reintroduced prey. By exposing reintroduced prey to carefully controlled levels of alien predators, in situ predation could enhance reintroduction success by facilitating acquisition of learned antipredator responses and through natural selection for appropriate antipredator traits. This in situ predator exposure should be viewed as a long-term process but is likely to be the most efficient and expedient way to improve prey responses and assist in broadscale recovery of threatened species.

Tailoring release protocols to individual species and sites: one size does not fit all.

Reintroduction programs for threatened species often include elaborate release strategies designed to improve success, but their advantages are rarely tested scientifically. We used a set of four experiments to demonstrate that the influence of release strategies on short-term reintroduction outcomes is related to both intrinsic and extrinsic factors. We compared different reintroduction strategies for three mammal species in an arid environment where exotic mammalian predators were removed. Wild greater stick-nest rats selected vegetation shelter sites with greater structural density than captive-bred rats, travelled further from the release site and experienced lower rates of mortality. In comparison, there was no difference in mortality or movement between wild and captive-bred greater bilbies. Burrowing bettongs and greater bilbies were also subjected to immediate and delayed release strategies and whilst no difference was detected in bilbies, bettongs that were subjected to delayed releases lost less weight and took less time to establish burrows than those that were immediately released. Interspecific differences in treatment response were attributed to predation risk, the nature of the release site, and behavioural traits such as shelter investment and sociality. Our varied results highlight the inadequacies of review articles focusing on optimum release protocols due to their attempt to generalise across species and release sites. We provide an example of a predictive model to guide future release strategy experimentation that recognises the range of intrinsic and extrinsic factors influencing reintroduction outcomes. We encourage researchers to treat programs experimentally, identify individual site and species characters that may influence release strategies and record data on movements, mortality, weight dynamics, and settling times and distances. The inherent issues of small sample size and low statistical power that plague most reintroduction experiments suggests there is also a need for increased standardisation and publication of data sets to enable appropriate meta-analyses to occur.