Analyzing captive breeding outcomes to inform reintroduction practice: lessons from the pookila (Pseudomys novaehollandiae).

Captive breeding is often used to produce individuals for reintroduction programs in order to reestablish a species in an area where it has become locally extinct. To maximize the likelihood of establishing a self-sustaining population in the wild, an analysis of data from captive breeding programs is commonly undertaken to (1) increase the quantity of individuals and rate at which they can be released, and (2) maintain or improve the genetic and phenotypic quality of individuals. Here we demonstrate how the knowledge gained from these analyses can also be applied to decision-making during the design of subsequent reintroductions to further advance a reintroduction program toward success. We conducted an analysis of data from a captive breeding program for the threatened pookila (Pseudomys novaehollandiae, New Holland mouse) spanning 6 years. We found evidence for relationships between the reproductive output of pookila and behavioral, demographic, experiential, health, and physiological predictors. Based on a biological interpretation of these results, and with reference to a checklist of all known translocation tactics, we recommend 11 specific design elements to maximize the probability of pookila reproduction postrelease (thereby improving the likelihood of reintroduction success). These recommendations should be interpreted as hypotheses to be evaluated and refined in future reintroduction trials for the pookila. The uncertainty around the postrelease survival and reproduction of a species that is common in reintroduction practice warrants the creative use of existing data to inform adaptive management. Indeed, there is a wealth information in well-kept captive breeding records that is currently underused by reintroduction practitioners. The direct integration of knowledge derived from captive breeding (where available) with decision-making for reintroductions, as described here, will help navigate these uncertainties, which would benefit the conservation of both understudied and well-known species around the world.

Mini Safe Havens for population recovery and reintroductions 'beyond-the-fence'.

In response to the ongoing decline of fauna worldwide, there has been growing interest in the rewilding of whole ecosystems outside of fenced sanctuaries or offshore islands. This interest will inevitably result in attempts to restore species where eliminating threats from predators and competitors is extremely challenging or impossible, or reintroductions of predators that will increase predation risk for extant prey (i.e., coexistence conservation). We propose 'Mini Safe Havens' (MSHs) as a potential tool for managing these threats. Mini Safe Havens are refuges that are permanently permeable to the focal species; allowing the emigration of individuals while maintaining gene flow through the boundary. Crucial to the effectiveness of the approach is the ongoing maintenance and monitoring required to preserve a low-to-zero risk of key threats within the MSH; facilitating in-situ learning and adaptation by focal species to these threats, at a rate and intensity of exposure determined by the animals themselves. We trialled the MSH approach for a pilot reintroduction of the Australian native New Holland mouse (Pseudomys novaehollandiae), in the context of a trophic rewilding project to address potential naïveté to a reintroduced native mammalian predator. We found that mice released into a MSH maintained their weight and continued to use the release site beyond 17 months (525 days) post-release. In contrast, individuals in temporary soft-release enclosures tended to lose weight and became undetectable approximately 1-month post-release. We discuss the broad applicability of MSHs for population recovery and reintroductions 'beyond-the-fence' and recommend avenues for further refinement of the approach. Supplementary Information: The online version contains supplementary material available at 10.1007/s10531-022-02495-6.

Ongoing declines of woodland birds: Are restoration plantings making a difference?

Woodland birds are a species assemblage of conservation concern, and their persistence in fragmented agricultural landscapes is dependent on both the preservation of existing woodland remnants and the implementation of restoration plantings. However, little is known about the habitat-use and persistence of birds in fragmented agricultural landscapes. We present a detailed, population-oriented study of woodland birds in temperate eucalypt woodland restoration plantings and remnant woodland patches in the South-west Slopes bioregion of New South Wales, Australia. First, we undertook a 3-yr mark-recapture project to assess annual survival and site fidelity in restoration plantings and woodland remnants. We supplemented our recapture efforts with resightings of color-banded individuals. Second, we tracked individual birds of two species, Superb Fairywren (Malurus cyaneus) and Willie Wagtail (Rhipidura leucophrys), and documented snapshots of their home ranges and movement patterns during the breeding season. Annual survival in the woodland bird assemblage was lower than expected (51%). Home ranges of the Superb Fairywren were positively correlated with patch size, and were constrained by patch edges in linear sites. Superb Fairywrens and Willie Wagtails were more likely to travel longer distances between substrates while foraging in linear sites. Willie Wagtails engaged in significant gap-crossing (up to 400 m) between adjacent habitat patches. Our findings indicate that (1) patch isolation and certain patch configurations place resident birds at an energetic disadvantage, and (2) in our study area, woodland bird populations are continuing to decline. We recommend landscape-scale habitat restoration programs aim to address ongoing population declines. Studies such as ours conducted over longer time periods would provide a deeper understanding of habitat use and population processes of woodland birds in fragmented agricultural landscapes.

Revegetation and reproduction: do restoration plantings in agricultural landscapes support breeding populations of woodland birds?

Restoration plantings are frequently occupied by native wildlife, but little is known about how planting attributes influence breeding by, and persistence of, fauna populations. We monitored breeding success of woodland birds in restoration plantings in a fragmented agricultural landscape in south-eastern Australia. We documented nest fate and daily nest survival (DSR) in plantings and remnant woodland sites. We analysed the influence on breeding success of patch attributes (size, shape, type) compared to other potentially influential predictors such as nest-site and microhabitat variables. We found that, in general, patch attributes did not play a significant role in determining breeding success for woodland birds. However, we examined a subset of species of conservation concern, and found higher DSR for these species in restoration plantings than in similarly sized woodland remnants. We also found negative effects of patch size and linearity on DSR in species of conservation concern. The primary cause of nest failure was predation (91%). We used camera trap imagery to identify the most common nest predators in our study sites: native predatory bird species, and the introduced red fox (Vulpes vulpes). Our findings are further evidence of the value of restoration plantings and small habitat patches for bird populations in fragmented agricultural landscapes. We recommend controlling for foxes to maximise the likelihood that restoration plantings and other woodland patches in Australia support breeding populations of woodland birds. More broadly, our study highlights the importance of taking a detailed, population-oriented approach to understanding factors that influence habitat suitability for fauna of conservation concern.

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.

Relationship between effective and demographic population size in continuously distributed populations.

Genetic monitoring of wild populations can offer insights into demographic and genetic information simultaneously. However, widespread application of genetic monitoring is hindered by large uncertainty in the estimation and interpretation of target metrics such as contemporary effective population size, Ne . We used four long-term genetic and demographic studies (≥9 years) to evaluate the temporal stability of the relationship between Ne and demographic population size (Nc ). These case studies focused on mammals that are continuously distributed, yet dispersal-limited within the spatial scale of the study. We estimated local, contemporary Ne with single-sample methods (LDNE, Heterozygosity Excess, and Molecular Ancestry) and demographic abundance with either mark-recapture estimates or catch-per-unit effort indices. Estimates of Ne varied widely within each case study suggesting interpretation of estimates is challenging. We found inconsistent correlations and trends both among estimates of Ne and between Ne and Nc suggesting the value of Ne as an indicator of Nc is limited in some cases. In the two case studies with consistent trends between Ne and Nc , FIS was more stable over time and lower, suggesting FIS may be a good indicator that the population was sampled at a spatial scale at which genetic structure is not biasing estimates of Ne . These results suggest that more empirical work on the estimation of Ne in continuous populations is needed to understand the appropriate context to use LDNe as a useful metric in a monitoring programme to detect temporal trends in either Ne or Nc .

Disease-associated change in an amphibian life-history trait.

Emerging pathogens can drive evolutionary shifts in host life-history traits, yet this process remains poorly documented in vertebrate hosts. Amphibian chytridiomycosis, caused by infection with the fungal pathogen Batrachochytrium dendrobatidis (Bd), is the worst recorded wildlife disease and has caused the extinction of over 100 species across multiple continents. A similar number of additional species have experienced mass declines and Bd remains a major source of mortality in many populations of declined species now persisting with the pathogen. Life-history theory predicts that increased extrinsic mortality in Bd-infected populations may alter amphibian life-history traits, but this has not been examined. Here, we investigate whether population Bd status is associated with age and size at maturity by comparing long-exposed Bd-infected populations, Bd-free populations, and museum specimens collected prior to Bd emergence for the endangered Australian frog Litoria verreauxii alpina. We show that Bd-infected populations have a higher proportion of males that mature at 1 year of age, and females that mature at 2 years of age, compared to Bd-free populations. Earlier maturation was associated with reduced size at maturity in males. Consistent with life-history theory, our findings may represent an adaptive evolutionary shift towards earlier maturation in response to high Bd-induced mortality. To our knowledge, this study provides the first evidence for a post-metamorphic Bd-associated shift in an amphibian life-history trait. Given high mortality in other Bd-challenged species, we suggest that chytridiomycosis may be a substantial new selection pressure shaping life-history traits in impacted amphibian species across multiple continents.

High adult mortality in disease-challenged frog populations increases vulnerability to drought.

Pathogen emergence can drive major changes in host population demography, with implications for population dynamics and sensitivity to environmental fluctuations. The amphibian disease chytridiomycosis, caused by infection with the fungal pathogen Batrachochytrium dendrobatidis (Bd), is implicated in the severe decline of over 200 amphibian species. In species that have declined but not become extinct, Bd persists and can cause substantial ongoing mortality. High rates of mortality associated with Bd may drive major changes in host demography, but this process is poorly understood. Here, we compared population age structure of Bd-infected populations, Bd-free populations and museum specimens collected prior to Bd emergence for the endangered Australian frog, Litoria verreauxii alpina (alpine tree frog). We then used population simulations to investigate how pathogen-associated demographic shifts affect the ability of populations to persist in stochastic environments. We found that Bd-infected populations have a severely truncated age structure associated with very high rates of annual adult mortality. Near-complete annual adult turnover in Bd-infected populations means that individuals breed once, compared with Bd-free populations where adults may breed across multiple years. Our simulations showed that truncated age structure erodes the capacity of populations to withstand periodic recruitment failure; a common challenge for species reproducing in uncertain environments. We document previously undescribed demographic shifts associated with a globally emerging pathogen and demonstrate how these shifts alter host ecology. Truncation of age structure associated with Bd effectively reduces host niche width and can help explain the contraction of L. v. alpina to perennial waterbodies where the risk of drought-induced recruitment failure is low. Reduced capacity to tolerate other sources of mortality may explain variation in decline severity among other chytridiomycosis-challenged species and highlights the potential to mitigate disease impacts through minimizing other sources of mortality.

Text analysis tools for identification of emerging topics and research gaps in conservation science.

Keeping track of conceptual and methodological developments is a critical skill for research scientists, but this task is increasingly difficult due to the high rate of academic publication. As a crisis discipline, conservation science is particularly in need of tools that facilitate rapid yet insightful synthesis. We show how a common text-mining method (latent Dirichlet allocation, or topic modeling) and statistical tests familiar to ecologists (cluster analysis, regression, and network analysis) can be used to investigate trends and identify potential research gaps in the scientific literature. We tested these methods on the literature on ecological surrogates and indicators. Analysis of topic popularity within this corpus showed a strong emphasis on monitoring and management of fragmented ecosystems, while analysis of research gaps suggested a greater role for genetic surrogates and indicators. Our results show that automated text analysis methods need to be used with care, but can provide information that is complementary to that given by systematic reviews and meta-analyses, increasing scientists' capacity for research synthesis.

Fine-scale refuges can buffer demographic and genetic processes against short-term climatic variation and disturbance: a 22-year case study of an arboreal marsupial.

Ecological disturbance and climate are key drivers of temporal dynamics in the demography and genetic diversity of natural populations. Microscale refuges are known to buffer species' persistence against environmental change, but the effects of such refuges on demographic and genetic patterns in response to short-term environmental variation are poorly understood. We quantified demographic and genetic responses of mountain brushtail possums (Trichosurus cunninghami) to rainfall variability (1992-2013) and to a major wildfire. We hypothesized that there would be underlying differences in demographic and genetic processes between an unburnt mesic refuge and a topographically exposed zone that was burnt in 2009. Fire caused a 2-year decrease in survival in the burnt zone, but the population grew after the fire due to immigration, leading to increased expected heterozygosity. We documented a fire-related behavioural shift, where the rate of movement by individuals in the unburnt refuge to the burnt zone decreased after fire. Irrespective of the fire, there were long-term differences in demographic and genetic parameters between the mesic/unburnt refuge and the nonmesic/burnt zone. Survival was high and unaffected by rainfall in the refuge, but lower and rainfall-dependent in the nonmesic zone. Net movement of individuals was directional, from the mesic refuge to the nonmesic zone, suggesting fine-scale source-sink dynamics. There were higher expected heterozygosity (HE ) and temporal genetic stability in the refuge, but lower HE and marked temporal genetic structure in the exposed habitat, consistent with reduced generational overlap caused by elevated mortality and immigration. Thus, fine-scale refuges can mediate the short-term demographic and genetic effects of climate and ecological disturbance.

Incorporating evolutionary processes into population viability models.

We examined how ecological and evolutionary (eco-evo) processes in population dynamics could be better integrated into population viability analysis (PVA). Complementary advances in computation and population genomics can be combined into an eco-evo PVA to offer powerful new approaches to understand the influence of evolutionary processes on population persistence. We developed the mechanistic basis of an eco-evo PVA using individual-based models with individual-level genotype tracking and dynamic genotype-phenotype mapping to model emergent population-level effects, such as local adaptation and genetic rescue. We then outline how genomics can allow or improve parameter estimation for PVA models by providing genotypic information at large numbers of loci for neutral and functional genome regions. As climate change and other threatening processes increase in rate and scale, eco-evo PVAs will become essential research tools to evaluate the effects of adaptive potential, evolutionary rescue, and locally adapted traits on persistence.

Breed locally, disperse globally: fine-scale genetic structure despite landscape-scale panmixia in a fire-specialist.

An exciting advance in the understanding of metapopulation dynamics has been the investigation of how populations respond to ephemeral patches that go 'extinct' during the lifetime of an individual. Previous research has shown that this scenario leads to genetic homogenization across large spatial scales. However, little is known about fine-scale genetic structuring or how this changes over time in ephemeral patches. We predicted that species that specialize on ephemeral habitats will delay dispersal to exploit natal habitat patches while resources are plentiful and thus display fine-scale structure. To investigate this idea, we evaluated the effect of frequent colonization of ephemeral habitats on the fine-scale genetic structure of a fire specialist, the black-backed woodpecker (Picoides arcticus) and found a pattern of fine-scale genetic structure. We then tested for differences in spatial structure between sexes and detected a pattern consistent with male-biased dispersal. We also detected a temporal increase in relatedness among individuals within newly burned forest patches. Our results indicate that specialist species that outlive their ephemeral patches can accrue significant fine-scale spatial structure that does not necessarily affect spatial structure at larger scales. This highlights the importance of both spatial and temporal scale considerations in both sampling and data interpretation of molecular genetic results.

Incest versus abstinence: reproductive trade-offs between mate limitation and progeny fitness in a self-incompatible invasive plant.

Plant mating systems represent an evolutionary and ecological trade-off between reproductive assurance through selfing and maximizing progeny fitness through outbreeding. However, many plants with sporophytic self-incompatibility systems exhibit dominance interactions at the S-locus that allow biparental inbreeding, thereby facilitating mating between individuals that share alleles at the S-locus. We investigated this trade-off by estimating mate availability and biparental inbreeding depression in wild radish from five different populations across Australia. We found dominance interactions among S-alleles increased mate availability relative to estimates based on individuals that did not share S-alleles. Twelve of the sixteen fitness variables were significantly reduced by inbreeding. For all the three life-history phases evaluated, self-fertilized offspring suffered a greater than 50% reduction in fitness, while full-sib and half-sib offspring suffered a less than 50% reduction in fitness. Theory indicates that fitness costs greater than 50% can result in an evolutionary trajectory toward a stable state of self-incompatibility (SI). This study suggests that dominance interactions at the S-locus provide a possible third stable state between SI and SC where biparental inbreeding increases mate availability with relatively minor fitness costs. This strategy allows weeds to establish in new environments while maintaining a functional SI system.

Do male and female black-backed woodpeckers respond differently to gaps in habitat?

We used population- and individual-based genetic approaches to assess barriers to movement in black-backed woodpeckers (Picoides arcticus), a fire-specialist that mainly occupies the boreal forest in North America. We tested if male and female woodpeckers exhibited the same movement patterns using both spatially implicit and explicit genetic analyses to define population structure and movement patterns of both sexes among populations. Three genetic groups were identified, a large, genetically continuous population that spans from the Rocky Mountains to Quebec, a small isolated population in South Dakota and a separate population in the western portion of their distribution (Oregon). Patterns of genetic diversity suggest extensive gene flow mediated by both males and females within the continuous boreal forest. However, male-mediated gene flow is the main form of connectivity between the continuously distributed group and the smaller populations of South Dakota and Oregon that are separated by large areas of unforested habitat, which apparently serves as a barrier to movement of female woodpeckers.