A comparison of pedigree, genetic and genomic estimates of relatedness for informing pairing decisions in two critically endangered birds: Implications for conservation breeding programmes worldwide.

Conservation management strategies for many highly threatened species include conservation breeding to prevent extinction and enhance recovery. Pairing decisions for these conservation breeding programmes can be informed by pedigree data to minimize relatedness between individuals in an effort to avoid inbreeding, maximize diversity and maintain evolutionary potential. However, conservation breeding programmes struggle to use this approach when pedigrees are shallow or incomplete. While genetic data (i.e., microsatellites) can be used to estimate relatedness to inform pairing decisions, emerging evidence indicates this approach may lack precision in genetically depauperate species, and more effective estimates will likely be obtained from genomic data (i.e., thousands of genome-wide single nucleotide polymorphisms, or SNPs). Here, we compare relatedness estimates and subsequent pairing decisions using pedigrees, microsatellites and SNPs from whole-genome resequencing approaches in two critically endangered birds endemic to New Zealand: kaki/black stilt (Himantopus novaezelandiae) and kakariki karaka/orange-fronted parakeet (Cyanoramphus malherbi). Our findings indicate that SNPs provide more precise estimates of relatedness than microsatellites when assessing empirical parent-offspring and full sibling relationships. Further, our results show that relatedness estimates and subsequent pairing recommendations using PMx are most similar between pedigree- and SNP-based approaches. These combined results indicate that in lieu of robust pedigrees, SNPs are an effective tool for informing pairing decisions, which has important implications for many poorly pedigreed conservation breeding programmes worldwide.

Reference Genomes from Distantly Related Species Can Be Used for Discovery of Single Nucleotide Polymorphisms to Inform Conservation Management.

Threatened species recovery programmes benefit from incorporating genomic data into conservation management strategies to enhance species recovery. However, a lack of readily available genomic resources, including conspecific reference genomes, often limits the inclusion of genomic data. Here, we investigate the utility of closely related high-quality reference genomes for single nucleotide polymorphism (SNP) discovery using the critically endangered kaki/black stilt (Himantopus novaezelandiae) and four Charadriiform reference genomes as proof of concept. We compare diversity estimates (i.e., nucleotide diversity, individual heterozygosity, and relatedness) based on kaki SNPs discovered from genotyping-by-sequencing and whole genome resequencing reads mapped to conordinal (killdeer, Charadrius vociferus), confamilial (pied avocet, Recurvirostra avosetta), congeneric (pied stilt, Himantopus himantopus) and conspecific reference genomes. Results indicate that diversity estimates calculated from SNPs discovered using closely related reference genomes correlate significantly with estimates calculated from SNPs discovered using a conspecific genome. Congeneric and confamilial references provide higher correlations and more similar measures of nucleotide diversity, individual heterozygosity, and relatedness. While conspecific genomes may be necessary to address other questions in conservation, SNP discovery using high-quality reference genomes of closely related species is a cost-effective approach for estimating diversity measures in threatened species.

A large-scale application of project prioritization to threatened species investment by a government agency.

In a global environment of increasing species extinctions and decreasing availability of funds with which to combat the causes of biodiversity loss, maximising the efficiency of conservation efforts is crucial. The only way to ensure maximum return on conservation investment is to incorporate the cost, benefit and likelihood of success of conservation actions into decision-making in a systematic and objective way. Here we report on the application of a Project Prioritization Protocol (PPP), first implemented by the New Zealand Government, to target and prioritize investment in threatened species in New South Wales, Australia, under the state's new Saving our Species program. Detailed management prescriptions for 368 threatened species were developed via an expert elicitation process, and were then prioritized using quantitative data on benefit, likelihood of success and implementation cost, and a simple cost-efficiency equation. We discuss the outcomes that have been realized even in the early stages of the program; including the efficient development of planning resources made available to all potential threatened species investors and the demonstration of a transparent and objective approach to threatened species management that will significantly increase the probability of meeting an objective to secure the greatest number of threatened species from extinction.

Spending limited resources on de-extinction could lead to net biodiversity loss.

There is contentious debate surrounding the merits of de-extinction as a biodiversity conservation tool. Here, we use extant analogues to predict conservation actions for potential de-extinction candidate species from New Zealand and the Australian state of New South Wales, and use a prioritization protocol to predict the impacts of reintroducing and maintaining populations of these species on conservation of extant threatened species. Even using the optimistic assumptions that resurrection of species is externally sponsored, and that actions for resurrected species can share costs with extant analogue species, public funding for conservation of resurrected species would lead to fewer extant species that could be conserved, suggesting net biodiversity loss. If full costs of establishment and maintenance for resurrected species populations were publicly funded, there could be substantial sacrifices in extant species conservation. If conservation of resurrected species populations could be fully externally sponsored, there could be benefits to extant threatened species. However, such benefits would be outweighed by opportunity costs, assuming such discretionary money could directly fund conservation of extant species. Potential sacrifices in conservation of extant species should be a crucial consideration in deciding whether to invest in de-extinction or focus our efforts on extant species.

Effect of risk aversion on prioritizing conservation projects.

Conservation outcomes are uncertain. Agencies making decisions about what threat mitigation actions to take to save which species frequently face the dilemma of whether to invest in actions with high probability of success and guaranteed benefits or to choose projects with a greater risk of failure that might provide higher benefits if they succeed. The answer to this dilemma lies in the decision maker's aversion to risk--their unwillingness to accept uncertain outcomes. Little guidance exists on how risk preferences affect conservation investment priorities. Using a prioritization approach based on cost effectiveness, we compared 2 approaches: a conservative probability threshold approach that excludes investment in projects with a risk of management failure greater than a fixed level, and a variance-discounting heuristic used in economics that explicitly accounts for risk tolerance and the probabilities of management success and failure. We applied both approaches to prioritizing projects for 700 of New Zealand's threatened species across 8303 management actions. Both decision makers' risk tolerance and our choice of approach to dealing with risk preferences drove the prioritization solution (i.e., the species selected for management). Use of a probability threshold minimized uncertainty, but more expensive projects were selected than with variance discounting, which maximized expected benefits by selecting the management of species with higher extinction risk and higher conservation value. Explicitly incorporating risk preferences within the decision making process reduced the number of species expected to be safe from extinction because lower risk tolerance resulted in more species being excluded from management, but the approach allowed decision makers to choose a level of acceptable risk that fit with their ability to accommodate failure. We argue for transparency in risk tolerance and recommend that decision makers accept risk in an adaptive management framework to maximize benefits and avoid potential extinctions due to inefficient allocation of limited resources.

Financial costs of meeting global biodiversity conservation targets: current spending and unmet needs.

World governments have committed to halting human-induced extinctions and safeguarding important sites for biodiversity by 2020, but the financial costs of meeting these targets are largely unknown. We estimate the cost of reducing the extinction risk of all globally threatened bird species (by ≥1 International Union for Conservation of Nature Red List category) to be U.S. $0.875 to $1.23 billion annually over the next decade, of which 12% is currently funded. Incorporating threatened nonavian species increases this total to U.S. $3.41 to $4.76 billion annually. We estimate that protecting and effectively managing all terrestrial sites of global avian conservation significance (11,731 Important Bird Areas) would cost U.S. $65.1 billion annually. Adding sites for other taxa increases this to U.S. $76.1 billion annually. Meeting these targets will require conservation funding to increase by at least an order of magnitude.

Pododermatitis in captive-reared black stilts (Himantopus novaezelandiae).

A potential cause of pododermatitis ("bumblefoot") was investigated in captive-reared juvenile black stilts at the Department of Conservation "Kaki Recovery Program" at Twizel, New Zealand. To address the importance of substrate, the development of clinical signs in individuals was compared among aviaries that contained rubber matting and/or salt footbaths, and controls. No effect of either experimental manipulation of the environment was apparent on pododermatitis development. With the substrate appearing not to be an initiating factor, and a previous study that indicated that the birds' diet fulfills the nutritional requirements for rearing black stilts in captivity, results of this study suggest that insufficient space for exercise may instead be the cause.

Genetic analyses reveal hybridization but no hybrid swarm in one of the world's rarest birds.

Hybridization facilitated by human activities has dramatically altered the evolutionary trajectories of threatened taxa around the globe. Whereas introduced mammalian predators and widespread habitat loss and degradation clearly imperil the recovery and survival of the New Zealand endemic black stilt or kaki (Himantopus novaezelandiae), the risk associated with hybridization between this critically endangered endemic and its self-introduced congener, the pied stilt or poaka (Himantopus himantopus leucocephalus) is less clear. Here, we combine Bayesian admixture analyses of microsatellite data with mitochondrial DNA sequence data to assess the levels of hybridization and introgression between kaki and poaka. We show that birds classified as hybrids on the basis of adult plumage are indeed of hybrid origin and that hybridization between kaki and poaka is both extensive and bidirectional. Despite this, we found almost no evidence for introgression from poaka to kaki, thus negating the popular belief that kaki represent a hybrid swarm. To our knowledge, ours represents the first comprehensive study to document a lack of widespread introgression for a species at risk despite a recent history of extensive bidirectional human-induced hybridization. We attribute this rather surprising result, in part, to reduced reproductive success in female hybrids combined with a transient male-biased kaki sex ratio. To maximize the evolutionary potential of kaki, we use these data to recommend conservation management activities aimed to maintain the genetic integrity and to maximize the genetic diversity of this iconic rare bird.

Optimal allocation of resources among threatened species: a project prioritization protocol.

Conservation funds are grossly inadequate to address the plight of threatened species. Government and conservation organizations faced with the task of conserving threatened species desperately need simple strategies for allocating limited resources. The academic literature dedicated to systematic priority setting usually recommends ranking species on several criteria, including level of endangerment and metrics of species value such as evolutionary distinctiveness, ecological importance, and social significance. These approaches ignore 2 crucial factors: the cost of management and the likelihood that the management will succeed. These oversights will result in misallocation of scarce conservation resources and possibly unnecessary losses. We devised a project prioritization protocol (PPP) to optimize resource allocation among New Zealand's threatened-species projects, where costs, benefits (including species values), and the likelihood of management success were considered simultaneously. We compared the number of species managed and the expected benefits gained with 5 prioritization criteria: PPP with weightings based on species value; PPP with species weighted equally; management costs; species value; and threat status. We found that the rational use of cost and success information substantially increased the number of species managed, and prioritizing management projects according to species value or threat status in isolation was inefficient and resulted in fewer species managed. In addition, we found a clear trade-off between funding management of a greater number of the most cost-efficient and least risky projects and funding fewer projects to manage the species of higher value. Specifically, 11 of 32 species projects could be funded if projects were weighted by species value compared with 16 projects if projects were not weighted. This highlights the value of a transparent decision-making process, which enables a careful consideration of trade-offs. The use of PPP can substantially improve conservation outcomes for threatened species by increasing efficiency and ensuring transparency of management decisions.

Developing the science of reintroduction biology.

With recent increases in the numbers of species reintroduction projects and reintroduction-related publications, there is now a recognizable field of reintroduction biology. Nevertheless, research thus far has been fragmented and ad hoc, rather than an organized attempt to gain reliable knowledge to improve reintroduction success. We reviewed 454 recent (1990-2005) peer-reviewed papers dealing with wildlife reintroductions from 101 journals. Most research has been retrospective, either opportunistic evaluations of techniques or general project summaries, and most inference is gained from post hoc interpretation of monitoring results on a species-by-species basis. Documentation of reintroduction outcomes has improved, however, and the derivation of more general principles via meta-analyses is expected to increase. The fragmentation of the reintroduction literature remains an obstacle. There is scope to improve reintroduction biology by greater application of the hypothetico-deductive method, particularly through the use of modeling approaches and well-designed experiments. Examples of fruitful approaches in reintroduction research include experimental studies to improve outcomes from the release of captive-bred animals, use of simulation modeling to identify factors affecting the viability of reintroduced populations, and the application of spatially explicit models to plan for and evaluate reintroductions. We recommend that researchers contemplating future reintroductions carefully determine a priori the specific goals, overall ecological purpose, and inherent technical and biological limitations of a given reintroduction and that evaluation processes incorporate both experimental and modeling approaches. We suggest that the best progress will be made when multidisciplinary teams of resource managers and scientists work in close collaboration and when results from comparative analyses, experiments, and modeling are combined within and among studies.