Developments in amphibian captive breeding and reintroduction programs

Captive breeding and reintroduction remain high profile but controversial conservation interventions. It is important to understand how such programs develop and respond to strategic conservation initiatives. We analyzed the contribution to conservation made by amphibian captive breeding and reintroduction since the launch of the International Union for Conservation of Nature (IUCN) Amphibian Conservation Action Plan (ACAP) in 2007. We assembled data on amphibian captive breeding and reintroduction from a variety of sources including the Amphibian Ark database and the IUCN Red List. We also carried out systematic searches of Web of Science, JSTOR, and Google Scholar for relevant literature. Relative to data collected from 1966 to 2006, the number of species involved in captive breeding and reintroduction projects increased by 57% in the 7 years since release of the ACAP. However, there have been relatively few new reintroductions over this period; most programs have focused on securing captive‐assurance populations (i.e., species taken into captivity as a precaution against extinctions in the wild) and conservation‐related research. There has been a shift to a broader representation of frogs, salamanders, and caecilians within programs and an increasing emphasis on threatened species. There has been a relative increase of species in programs from Central and South America and the Caribbean, where amphibian biodiversity is high. About half of the programs involve zoos and aquaria with a similar proportion represented in specialist facilities run by governmental or nongovernmental agencies. Despite successful reintroduction often being regarded as the ultimate milestone for such programs, the irreversibility of many current threats to amphibians may make this an impractical goal. Instead, research on captive assurance populations may be needed to develop imaginative solutions to enable amphibians to survive alongside current, emerging, and future threats.     

Longitudinal monitoring of neutral and adaptive genomic diversity in a reintroduction

Restoration programs in the form of ex-situ breeding combined with reintroductions are becoming critical to counteract demographic declines and species losses. Such programs are increasingly using genetic management to improve conservation outcomes. However, the lack of long-term monitoring of genetic indicators following reintroduction prevents assessments of the trajectory and persistence of reintroduced populations. We carried out an extensive monitoring program in the wild for a threatened small-bodied fish (southern pygmy perch, Nannoperca australis) to assess the long-term genomic effects of its captive breeding and reintroduction. The species was rescued prior to its extirpation from the terminal lakes of Australia's Murray-Darling Basin, and then used for genetically informed captive breeding and reintroductions. Subsequent annual or biannual monitoring of abundance, fitness, and occupancy over a period of 11 years, combined with postreintroduction genetic sampling, revealed survival and recruitment of reintroduced fish. Genomic analyses based on data from the original wild rescued, captive born, and reintroduced cohorts revealed low inbreeding and strong maintenance of neutral and candidate adaptive genomic diversity across multiple generations. An increasing trend in the effective population size of the reintroduced population was consistent with field monitoring data in demonstrating successful re-establishment of the species. This provides a rare empirical example that the adaptive potential of a locally extinct population can be maintained during genetically informed ex-situ conservation breeding and reintroduction into the wild. Strategies to improve biodiversity restoration via ex-situ conservation should include genetic-based captive breeding and longitudinal monitoring of standing genomic variation in reintroduced populations.     

Designing the Ark: Setting Priorities for Captive Breeding

Zoos can help conserve only a small minority of the species threatened with extinction. Clear and rational criteria for identifying which threatened taxa zoos should focus on are therefore essential. Current priorities for ex situ conservation stress the importance of large vertebrates. We show that this hampers the efficient use of resources because such species are less likely to breed well in captivity than smaller-bodied taxa and, despite longer generation lengths, are more costly to maintain in long-term breeding programs. Moreover, although reintroduction to the wild frees zoo space for other species and is the ultimate aim of captive breeding, zoos show no tendency to target species for which continued habitat availability makes reintroduction a realistic prospect. We suggest that zoos adopt selection criteria that reflect the economic and biological realities of captive breeding and reintroduction if they are to maximize their contribution to species conservation, and we present data on the preferences of zoo visitors indicating that doing so need not adversely affect zoo attendance.     

Phylogenetic Reanalysis of the Saudi Gazelle and Its Implications for Conservation

Abstract: The identification of taxonomically appropriate populations of endangered species for captive breeding and reintroduction programs is fundamental to the success of those programs. The Saudi gazelle (   Gazella saudiya ) was endemic to the Arabian peninsula but is now considered extinct in the wild and is potentially a candidate for captive breeding and reintroduction. Using 375 base pairs of mitochondrial DNA (mtDNA) cytochrome b gene derived from museum samples collected from the wild prior to the presumed extinction of this species, we show that G. saudiya is the sister taxon of the African dorcas gazelle (  G. dorcas ). Reciprocal monophyly of G. saudiya mtDNA haplotypes with G. dorcas , coupled with morphological distinctiveness, suggests that it is an evolutionarily significant unit. These data indicate that captive populations identified previously as potential sources of G. saudiya for captive breeding appear incorrectly designated and are irrelevant to the conservation of G. saudiya. The polymerase chain reaction–restriction fragment length polymorphism ( PCR-RFLP) analysis of several private collections of living gazelles in Saudi Arabia provides no evidence for the survival of G. saudiya. We recommend that field surveys be undertaken to establish whether G. saudiya is indeed extinct in the wild and that other private collections within the Arabian peninsula be screened genetically. We urge caution when captive animals of unknown provenance are used to investigate the phylogenetics of cryptic species groups.     

Selecting for Tolerance against Pathogens and Herbivores to Enhance Success of Reintroduction and Translocation

Abstract: Some species have insufficient defenses against climate change, emerging infectious diseases, and non‐native species because they have not been exposed to these factors over their evolutionary history, and this can decrease their likelihood of persistence. Captive breeding programs are sometimes used to reintroduce individuals back into the wild; however, successful captive breeding and reintroduction can be difficult because species or populations often cannot coexist with non‐native pathogens and herbivores without artificial selection. In captive breeding programs, breeders can select for host defenses that prevent or reduce pathogen or herbivore burden (i.e., resistance) or traits that limit the effects of parasitism or herbivory on host fitness (i.e., tolerance). We propose that selection for host tolerance may enhance the success of reintroduction or translocation because tolerant hosts generally have neutral effects on introduced pathogens and herbivores. The release of resistant hosts would have detrimental effects on their natural enemies, promoting rapid evolution to circumvent the host resistance that may reduce the long‐term probability of persistence of the reintroduced or translocated species. We examined 2 case studies, one on the pathogenic amphibian chytrid fungus ( Batrachochytrium dendrobatidis [Bd]) and the other on the herbivorous cactus moth ( Cactoblastis cactorum) in the United States, where it is not native. In each case study, we provide recommendations for how captive breeders and managers could go about selecting for host tolerance. Selecting for tolerance may offer a promising tool to rescue hosts species from invasive natural enemies as well as new natural enemies associated with climate change‐induced range shifts.     

A novel holistic framework for genetic‐based captive‐breeding and reintroduction programs

Research in reintroduction biology has provided a greater understanding of the often limited success of species reintroductions and highlighted the need for scientifically rigorous approaches in reintroduction programs. We examined the recent genetic‐based captive‐breeding and reintroduction literature to showcase the underuse of the genetic data gathered. We devised a framework that takes full advantage of the genetic data through assessment of the genetic makeup of populations before (past component of the framework), during (present component), and after (future component) captive‐breeding and reintroduction events to understand their conservation potential and maximize their success. We empirically applied our framework to two small fishes: Yarra pygmy perch (Nannoperca obscura) and southern pygmy perch (Nannoperca australis). Each of these species has a locally adapted and geographically isolated lineage that is endemic to the highly threatened lower Murray–Darling Basin in Australia. These two populations were rescued during Australia's recent decade‐long Millennium Drought, when their persistence became entirely dependent on captive‐breeding and subsequent reintroduction efforts. Using historical demographic analyses, we found differences and similarities between the species in the genetic impacts of past natural and anthropogenic events that occurred in situ, such as European settlement (past component). Subsequently, successful maintenance of genetic diversity in captivity—despite skewed brooder contribution to offspring—was achieved through carefully managed genetic‐based breeding (present component). Finally, genetic monitoring revealed the survival and recruitment of released captive‐bred offspring in the wild (future component). Our holistic framework often requires no additional data collection to that typically gathered in genetic‐based breeding programs, is applicable to a wide range of species, advances the genetic considerations of reintroduction programs, and is expected to improve with the use of next‐generation sequencing technology.     

Limited contributions of released animals from zoos to North American conservation translocations

With the loss of biodiversity accelerating, conservation translocations such as reintroductions are becoming an increasingly common conservation tool. Conservation translocations must source individuals for release from either wild or captive-bred populations. We asked what proportion of North American conservation translocations rely on captive breeding and to what extent zoos and aquaria (hereafter zoos) fulfill captive breeding needs. We searched for mention of captive breeding and zoo involvement in all 1863 articles included in the North American Conservation Translocations database, which comprises journal articles and grey literature published before 2014 on conservation translocations in Canada, the United States, Mexico, the Caribbean, and Central America before 2014 as identified by a comprehensive literature review. Conservation translocations involved captive breeding for 162 (58%) of the 279 animal species translocated. Fifty-four zoos contributed animals for release. The 40 species of animals bred for release by zoos represented only 14% of all animal species for which conservation translocations were published and only 25% of all animal species that were bred for releases occurring in North America. Zoo contributions varied by taxon, ranging from zoo-bred animals released in 42% of amphibian conservation translocations to zero contributions for marine invertebrates. Proportional involvement of zoos in captive-breeding programs for release has increased from 1974 to 2014 (r = 0.325, p = 0.0313) as has the proportion of translocation-focused scientific papers coauthored by zoo professionals (from 0% in 1974 to 42% in 2013). Although zoos also contribute to conservation translocations through education, funding, and professional expertise, increasing the contribution of animals for release in responsible conservation translocation programs presents a future conservation need and opportunity. We especially encourage increased dialogue and planning between the zoo community, academic institutions, and governments to optimize the direct contribution zoos can make to wildlife conservation through conservation translocations.     

Demographic Models and Reality in Reintroductions: Persian Fallow Deer in Israel

Abstract:  Because most reintroduced species are rare, data on their dynamics are scarce. Consequently, reintroduction programs often rely on data from other species or captive populations to project the performance of the reintroduced population in the wild. We compared the reproductive success and survival of a Persian fallow deer ( Dama mesopotamica ) population reintroduced in Israel over the first 5 years of the project with the survival and reproduction parameters estimated while planning the reintroduction. In addition, we compared the actual growth of the wild population with the growth originally projected by a computer model in the original reintroduction program. We monitored 74 radio-collared individuals (57 females and 17 males) released semiannually 1996–2001. Survival during the first year after release was lower than later years (0.90 and 0.82 versus 0.95 and 0.88, for females and males, respectively). Such an impact was not anticipated in the original plan, but overall survival was higher than originally projected. As assumed in the reintroduction program, reproductive success improved significantly with time since release and overall, was higher than expected. The mean number of animals released annually was lower than planned. Overall, the growth of the reintroduced population was slower than projected, but the deviation was close to confidence limits and the pattern similar. After 5 years it appears that the original time frame of 8–10 years for project completion can be met or at worst will cause a 1-year delay. Over the short term of 5 years, projection models in reintroduction programs are useful tools for assessing the sustained use of the breeding core, depicting the dynamics of the population in the wild, providing a relatively accurate time frame for the successful completion of the project, and assessing project success.     

Critically evaluating best management practices for preventing freshwater turtle extinctions

Ex situ conservation tools, such as captive breeding for reintroduction, are considered a last resort to recover threatened or endangered species, but they may also help reduce anthropogenic threats where it is difficult or impossible to address them directly. Headstarting, or captive rearing of eggs or neonate animals for subsequent release into the wild, is controversial because it treats only a symptom of a larger conservation problem; however, it may provide a mechanism to address multiple threats, particularly near population centers. We conducted a population viability analysis of Australia's most widespread freshwater turtle, Chelodina longicollis, to determine the effect of adult roadkill (death by collision with motor vehicles), which is increasing, and reduced recruitment through nest predation from introduced European red foxes (Vulpes vulpes). We also modeled management scenarios to test the effectiveness of headstarting, fox management, and measures to reduce mortality on roads. Only scenarios with headstarting from source populations eliminated all risks of extinction and allowed population growth. Small increases in adult mortality (2%) had the greatest effect on population growth and extinction risk. Where threats simultaneously affected other life‐history stages (e.g., recruitment), eliminating harvest pressures on adult females alone did not eliminate the risk of population extinction. In our models, one source population could supply enough hatchlings annually to supplement 25 other similar‐sized populations such that extinction was avoided. Based on our results, we believe headstarting should be a primary tool for managing freshwater turtles for which threats affect multiple life‐history stages. We advocate the creation of source populations for managing freshwater turtles that are greatly threatened at multiple life‐history stages, such as depredation of eggs by invasive species and adult mortality via roadkill.     

Guidelines for Subspecific Substitutions in Wildlife Restoration Projects

Reintroduction of animals is becoming increasingly popular as a means of restoring populations of threatened species. Sometimes depletion of wild populations leaves only captive populations from which reintroduction projects can obtain founders for releases. The World Conservation Union guidelines on reintroductions recommend that the individuals to be reintroduced should be of the same subspecies as those that were extirpated. In some cases, however, a subspecies may have become extinct in the wild and in captivity. A substitute form may then be chosen for possible release. Such substitutions are actually a form of benign introduction. Considerations include assessment of the value of a substitution project and the selection of a suitable substitute. Species substitutions increase biodiversity, conserve related forms, improve public awareness of conservation issues, educate the public, and may be implemented for aesthetic or economic reasons. Selection of a suitable substitute should focus on extant subspecies and consider genetic relatedness, phenotype, ecological compatibility, and conservation value of potential candidates. An example of a substitution project is the reintroduction of the North African Red-necked Ostrich (  Struthio camelus camelus ) into areas once occupied by the now extinct Arabian Ostrich (  Struthio camelus syriacus ). S. c. camelus was chosen as a substitute because of its geographic proximity, phenotypic similarity, and conservation value. The World Conservation Union's reintroduction guidelines should be consulted before a project is begun.     

Assessing the global zoo response to the amphibian crisis through 20‐year trends in captive collections

Global amphibian declines are one of the biggest challenges currently facing the conservation community, and captive breeding is one way to address this crisis. Using information from the International Species Information System zoo network, we examined trends in global zoo amphibian holdings across species, zoo region, and species geographical region of origin from 1994 to 2014. These trends were compared before and after the 2004 Global Amphibian Assessment to assess whether any changes occurred and whether zoo amphibian conservation effort had increased. The numbers of globally threatened species (GTS) and their proportional representation in global zoo holdings increased and this rate of increase was significantly greater after 2004. North American, European, and Oceanian GTS were best represented in zoos globally, and proportions of Oceanian GTS held increased the most since 2004. South American and Asian GTS had the lowest proportional representation in zoos. At a regional zoo level, European zoos held the lowest proportions of GTS, and this proportion did not increase after 2004. Since 1994, the number of species held in viable populations has increased, and these species are distributed among more institutions. However, as of 2014, zoos held 6.2% of globally threatened amphibians, a much smaller figure than for other vertebrate groups and one that falls considerably short of the number of species for which ex situ management may be desirable. Although the increased effort zoos have put into amphibian conservation over the past 20 years is encouraging, more focus is needed on ex situ conservation priority species. This includes building expertise and capacity in countries that hold them and tracking existing conservation efforts if the evidence‐based approach to amphibian conservation planning at a global level is to be further developed.     

Founder Effects,Inbreeding, and Loss of Genetic Diversity in Four Avian Reintroduction Programs

Abstract: The number of individuals translocated and released as part of a reintroduction is often small, as is the final established population, because the reintroduction site is typically small. Small founder and small resulting populations can result in population bottlenecks, which are associated with increased rates of inbreeding and loss of genetic diversity, both of which can affect the long‐term viability of reintroduced populations. I used information derived from pedigrees of four monogamous bird species reintroduced onto two different islands (220 and 259 ha) in New Zealand to compare the pattern of inbreeding and loss of genetic diversity among the reintroduced populations. Although reintroduced populations founded with few individuals had higher levels of inbreeding, as predicted, other factors, including biased sex ratio and skewed breeding success, contributed to high levels of inbreeding and loss of genetic diversity. Of the 10–58 individuals released, 4–25 genetic founders contributed at least one living descendent and yielded approximately 3–11 founder–genome equivalents (number of genetic founders assuming an equal contribution of offspring and no random loss of alleles across generations) after seven breeding seasons. This range is much lower than the 20 founder–genome equivalents recommended for captive‐bred populations. Although the level of inbreeding in one reintroduced population initially reached three times that of a closely related species, the long‐term estimated rate of inbreeding of this one population was approximately one‐third that of the other species due to differences in carrying capacities of the respective reintroduction sites. The increasing number of reintroductions to suitable areas that are smaller than those I examined here suggests that it might be useful to develop long‐term strategies and guidelines for reintroduction programs, which would minimize inbreeding and maintain genetic diversity.     

Biological parameters used in setting captive‐breeding quotas for Indonesia's breeding facilities

The commercial captive breeding of wildlife is often seen as a potential conservation tool to relieve pressure on wild populations, but laundering of wild‐sourced specimens as captive bred can seriously undermine conservation efforts and provide a false sense of sustainability. Indonesia is at the center of such controversy; therefore, we examined Indonesia's captive‐breeding production plan (CBPP) for 2016. We compared the biological parameters used in the CBPP with parameters in the literature and with parameters suggested by experts on each species and identified shortcomings of the CBPP. Production quotas for 99 out of 129 species were based on inaccurate or unrealistic biological parameters and production quotas deviated more than 10% from what parameters in the literature allow for. For 38 species, the quota exceeded the number of animals that can be bred based on the biological parameters (range 100–540%) calculated with equations in the CBPP. We calculated a lower reproductive output for 88 species based on published biological parameters compared with the parameters used in the CBPP. The equations used in the production plan did not appear to account for other factors (e.g., different survival rate for juveniles compared to adult animals) involved in breeding the proposed large numbers of specimens. We recommend the CBPP be adjusted so that realistic published biological parameters are applied and captive‐breeding quotas are not allocated to species if their captive breeding is unlikely to be successful or no breeding stock is available. The shortcomings in the current CBPP create loopholes that mean mammals, reptiles, and amphibians from Indonesia declared captive bred may have been sourced from the wild.     

Linking Wild and Captive Populations to Maximize Species Persistence: Optimal Translocation Strategies

Abstract:  Captive breeding of animals is widely used to manage endangered species, frequently with the ambition of future reintroduction into the wild. Because this conservation measure is very expensive, we need to optimize decisions, such as when to capture wild animals or release captive-bred individuals into the wild. It is unlikely that one particular strategy will always work best; instead, we expect the best decision to depend on the number of individuals in the wild and in captivity. We constructed a first-order Markov-chain population model for two populations, one captive and one wild, and we used stochastic dynamic programming to identify optimal state-dependent strategies. The model recommends unique sequences of optimal management actions over several years. A robust rule of thumb for species that can increase faster in captivity than in the wild is to capture the entire wild population whenever the wild population is below a threshold size of 20 females. This rule applies even if the wild population is growing and under a broad range of different parameter values. Once a captive population is established, it should be maintained as a safety net and animals should be released only if the captive population is close to its carrying capacity. We illustrate the utility of this model by applying it to the Arabian oryx ( Oryx leucoryx ). The threshold for capturing the entire Arabian oryx population in the wild is 36 females, and captive-bred individuals should not be released before the captive facilities are at least 85% full.     

Effects of a Proposed Ex Situ Conservation Program on In Situ Conservation of the Babirusa, an Endangered Suid

Abstract: Detailed data are rarely available to show how interventions such as captive breeding programs can create an uncontrolled demand for live specimens of endangered species. We present a case study of the effect of a planned, internationally recognized captive breeding program on trade in the endangered babirusa wild pig from July to December 1998. Although the program had not yet begun, international interest in the captive breeding of babirusas gave hunters and dealers the false impression that there was a potentially lucrative and officially sanctioned national and international demand for any live babirusas they might catch. Swift action by the Indonesian authorities halted this trade, but the study provides a warning about the damage that can be caused to the conservation of a species if management programs are instituted without a full understanding of the practicalities of its conservation, particularly interactions between the species and local people.     

Species Review of Amphibian Extinction Risks in Madagascar: Conclusions from the Global Amphibian Assessment

Abstract:  We assessed the extinction risks of Malagasy amphibians by evaluating their distribution, occurrence in protected areas, population trends, habitat quality, and prevalence in commercial trade. We estimated and mapped the distribution of each of the 220 described Malagasy species and applied, for the first time, the IUCN Red List categories and criteria to all species described at the time of the assessment. Nine species were categorized as critically endangered, 21 as endangered, and 25 as vulnerable. The most threatened species occur on the High Plateau and/or have been subjected to overcollection for the pet trade, but restricted extent of occurrence and ongoing habitat destruction were identified as the most important factors influencing extinction threats. The two areas with the majority of threatened species were the northern Tsaratanana-Marojejy-Masoala highlands and the southeastern Anosy Mountains. The current system of protected areas includes 82% of the threatened amphibian species. Of the critically endangered species, 6 did not occur in any protected area. For conservation of these species we recommend the creation of a reserve for the species of the Mantella aurantiaca group, the inclusion of two Scaphiophryne species in the Convention on the International Trade in Endangered Species Appendix II, and the suspension of commercial collecting for Mantella cowani . Field surveys during the last 15 years reveal no pervasive extinction of Malagasy amphibians resulting from disease or other agents, as has been reported in some other areas of the world.     

Conservation Value of Non-Native Banteng in Northern Australia

Abstract:  The global species extinction crisis has provided the impetus for elaborate translocation, captive breeding, and cloning programs, but more extreme actions may be necessary. We used mitochondrial DNA, Y-chromosome, and nuclear lactoferrin-encoding gene sequencing to identify a wild population of a pure-strain endangered bovid ( Bos javanicus ) introduced into northern Australia over 150 years ago. This places the Australian population in a different conservation category relative to its domesticated conspecific in Indonesia (i.e., Bali cattle) that has varying degrees of introgression from other domesticated Bos spp. The success of this endangered non-native species demonstrates that although risky, the deliberate introduction of threatened exotic species into non-native habitat may provide, under some circumstances, a biologically feasible option for conserving large herbivores otherwise imperiled in their native range.     

Inbreeding and Loss of Genetic Variation in a Reintroduced Population of Mauritius Kestrel

Abstract:  Many populations have recovered from severe bottlenecks either naturally or through intensive conservation management. In the past, however, few conservation programs have monitored the genetic health of recovering populations. We conducted a conservation genetic assessment of a small, reintroduced population of Mauritius Kestrel ( Falco punctatus ) to determine whether genetic deterioration has occurred since its reintroduction. We used pedigree analysis that partially accounted for individuals of unknown origin to document that (1) inbreeding occurred frequently (2.6% increase per generation; N _eI= 18.9), (2) 25% of breeding pairs were composed of either closely or moderately related individuals, (3) genetic diversity has been lost from the population (1.6% loss per generation; N _eV= 32.1) less rapidly than the corresponding increase in inbreeding, and (4) ignoring the contribution of unknown individuals to a pedigree will bias the metrics derived from that pedigree, ultimately obscuring the prevailing genetic dynamics. The rates of inbreeding and loss of genetic variation in the subpopulation of Mauritius Kestrel we examined were extreme and among the highest yet documented in a wild vertebrate population. Thus, genetic deterioration may affect this population's long-term viability. Remedial conservation strategies are needed to reduce the impact of inbreeding and loss of genetic variation in this species. We suggest that schemes to monitor genetic variation after reintroduction should be an integral component of endangered species recovery programs.     

Bibliometric investigation of the integration of animal personality in conservation contexts

Consistent individual differences in behavior, commonly termed animal personality, are a widespread phenomenon across taxa that have important consequences for fitness, natural selection, and trophic interactions. Animal personality research may prove useful in several conservation contexts, but which contexts remains to be determined. We conducted a structured literature review of 654 studies identified by combining search terms for animal personality and various conservation subfields. We scored the relevance of personality and conservation issues for each study to identify which studies meaningfully integrated the 2 fields as opposed to surface-level connections or vague allusions. We found a taxonomic bias toward mammals (29% of all studies). Very few amphibian or reptile studies applied personality research to conservation issues (6% each). Climate change (21%), invasive species (15%), and captive breeding and reintroduction (13%) were the most abundant conservation subfields that occurred in our search, though a substantial proportion of these papers weakly integrated conservation and animal personality (climate change 54%, invasive species 51%, captive breeding and reintroduction 40%). Based on our results, we recommend that researchers strive for consistent and broadly applicable terminology when describing consistent behavioral differences to minimize confusion and improve the searchability of research. We identify several gaps in the literature that appear to be promising and fruitful avenues for future research, such as disease transmission as a function of sociability or exploration as a driver of space use in protected areas. Practitioners can begin informing future conservation efforts with knowledge gained from animal personality research.     

Captive Breeding and Reintroduction Evaluation Criteria: a Case Study of Peninsular Bighorn Sheep

Abstract: Captive breeding and reintroduction programs are rarely evaluated, and assessment criteria vary widely. We used the following criteria to evaluate a bighorn sheep ( Ovis canadensis ) augmentation program: (1) survival and recruitment rates in the captive population, (2) survival of released animals, (3) recruitment of released animals, (4) growth rate of the reintroduced or augmented population, and (5) establishment of a viable wild population. Captive bighorn survival and recruitment was high, averaging 0.98 (SD = 0.05) and 71.0% (SD = 19.4), respectively. Annual survival of free-ranging captive-reared bighorn ( n = 73, x = 0.80, SD = 0.11) did not differ (   Z = −0.85, p = 0.40; n = 14) from survival of wild-reared bighorn ( n = 43, x = 0.81, SD = 0.12). Recruitment was unusually low for both captive-reared (  x = 13.7%, SD = 0.24) and wild-reared ewes (  x = 13.7%, SD = 0.20). Although reintroduction did not result in population growth or establishment of a viable population, it helped prevent extirpation of the reinforced deme, preserved metapopulation linkage, and aided habitat preservation. Chronic low recruitment and low adult survivorship precluded achievement of criteria 3–5. Environmental conditions in the release area also appeared to hinder program success. Standard evaluation criteria for ongoing reintroductions allow for informative assessments and facilitate comparisons needed to refine reintroduction science as a recovery tool for threatened or endangered populations.