Captive Breeding, Reintroduction, and the Conservation of Amphibians

Abstract: The global amphibian crisis has resulted in renewed interest in captive breeding as a conservation tool for amphibians. Although captive breeding and reintroduction are controversial management actions, amphibians possess a number of attributes that make them potentially good models for such programs. We reviewed the extent and effectiveness of captive breeding and reintroduction programs for amphibians through an analysis of data from the Global Amphibian Assessment and other sources. Most captive breeding and reintroduction programs for amphibians have focused on threatened species from industrialized countries with relatively low amphibian diversity. Out of 110 species in such programs, 52 were in programs with no plans for reintroduction that had conservation research or conservation education as their main purpose. A further 39 species were in programs that entailed captive breeding and reintroduction or combined captive breeding with relocations of wild animals. Nineteen species were in programs with relocations of wild animals only. Eighteen out of 58 reintroduced species have subsequently bred successfully in the wild, and 13 of these species have established self‐sustaining populations. As with threatened amphibians generally, amphibians in captive breeding or reintroduction programs face multiple threats, with habitat loss being the most important. Nevertheless, only 18 out of 58 reintroduced species faced threats that are all potentially reversible. When selecting species for captive programs, dilemmas may emerge between choosing species that have a good chance of surviving after reintroduction because their threats are reversible and those that are doomed to extinction in the wild as a result of irreversible threats. Captive breeding and reintroduction programs for amphibians require long‐term commitments to ensure success, and different management strategies may be needed for species earmarked for reintroduction and species used for conservation research and education.     

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.     

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.     

Role of Familiarity and Preference in Reproductive Success in Ex Situ Breeding Programs

Abstract: Success of captive‐breeding programs centers on consistent reproduction among captive animals. However, many individuals do not reproduce even when they are apparently healthy and presented with mates. Mate choice can affect multiple parameters of reproductive success, including mating success, offspring production, offspring survival, and offspring fecundity. We investigated the role of familiarity and preference on reproductive success of female Columbia Basin pygmy rabbits (Brachylagus idahoensis) as measured by litter production, litter size, average number of young that emerged from the burrow, and average number of young that survived to 1 year. We conducted these studies on pygmy rabbits at the Oregon Zoo (Portland, Oregon, U.S.A.) and Washington State University (Pullman, Washington, U.S.A.) from February to June 2006, 2007, and 2008. Before mating, we housed each female adjacent to 2 males (neighbors). Female preference for each potential mate was determined on the basis of behavioral interactions observed and measured between the rabbits. We compared reproductive success between females mated with neighbor and non‐neighbor males and between females mated with preferred and nonpreferred males. Our findings suggest that mating with a neighbor compared with a non‐neighbor and mating with a preferred neighbor compared with a nonpreferred neighbor increased reproductive success in female pygmy rabbits. Litter production, average number of young that emerged, and average number of young that survived to 1 year were higher in rabbits that were neighbors before mating than in animals who were not neighbors. Pairing rabbits with a preferred partner increased the probability of producing a litter and was significantly associated with increased litter size. In captive breeding programs, mates are traditionally selected on the basis of genetic parameters to minimize loss of genetic diversity and inbreeding coefficients. Our results suggest that integrating genetic information with social dynamics and behavioral measures of preference may increase the reproductive output of the pygmy rabbit captive‐breeding program. Our findings are consistent with the idea that allowing mate choice and familiarity increase the reproductive success of captive‐breeding programs for endangered species.     

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.     

Preserving Population Allele Frequencies in Ex Situ Conservation Programs

Abstract: Optimization of contributions of parents to progeny by minimizing the average coancestry of the progeny is an effective strategy for maintaining genetic diversity in ex situ conservation programs, but its application on the basis of molecular markers has the negative collateral effect of homogenizing the allelic frequencies at each locus. Because one of the objectives of a conservation program is to preserve the genetic composition of the original endangered population, we devised a method in which markers are used to maintain the allele frequency distribution at each locus as closely as possible to that of the native population. Contributions of parents were obtained so as to minimize changes in allele frequency for a set of molecular markers in a population of reduced size. We used computer simulations, under a range of scenarios, to assess the effectiveness of the method in comparison with methods in which contributions of minimum coancestry are sought, either making use of molecular markers or genealogical information. Our simulations indicated that the proposed method effectively maintained the original distribution of allele frequencies, particularly under strong linkage, and maintained acceptable levels of genetic diversity in the population. Nevertheless, contributions of minimum coancestry determined from pedigree information but ignoring the genealogy previous to the conservation program, was the most effective method for maintaining allelic frequencies in realistic situations.     

A role for selective contraception of individuals in conservation

Contraception has an established role in managing overabundant populations and preventing undesirable breeding in zoos. We propose that it can also be used strategically and selectively in conservation to increase the genetic and behavioral quality of the animals. In captive breeding programs, it is becoming increasingly important to maximize the retention of genetic diversity by managing the reproductive contribution of each individual and preventing genetically suboptimal breeding through the use of selective contraception. Reproductive suppression of selected individuals in conservation programs has further benefits of allowing animals to be housed as a group in extensive enclosures without interfering with breeding recommendations, which reduces adaptation to captivity and facilitates the expression of wild behaviors and social structures. Before selective contraception can be incorporated into a breeding program, the most suitable method of fertility control must be selected, and this can be influenced by factors such as species life history, age, ease of treatment, potential for reversibility, and desired management outcome for the individual or population. Contraception should then be implemented in the population following a step‐by‐step process. In this way, it can provide crucial, flexible control over breeding to promote the physical and genetic health and sustainability of a conservation dependent species held in captivity. For Tasmanian devils (Sarcophilus harrisii), black‐flanked rock wallabies (Petrogale lateralis), and burrowing bettongs (Bettongia lesueur), contraception can benefit their conservation by maximizing genetic diversity and behavioral integrity in the captive breeding program, or, in the case of the wallabies and bettongs, by reducing populations to a sustainable size when they become locally overabundant. In these examples, contraceptive duration relative to reproductive life, reversibility, and predictability of the contraceptive agent being used are important to ensure the potential for individuals to reproduce following cessation of contraception, as exemplified by the wallabies when their population crashed and needed females to resume breeding.     

Conservation Biology in Asia: the Major Policy Challenges

Abstract:  With about half the world's human population and booming economies, Asia faces numerous challenges to its biodiversity. The Asia Section of the Society for Conservation Biology has identified some key policy issues in which significant progress can be made. These include developing new sources of funding for forest conservation; identifying potential impacts of energy alternatives on the conservation of biodiversity; curbing the trade in endangered species of plants and animals; a special focus on the conservation of mountain biodiversity; enhancing relevant research; ensuring that conservation biology contributes to major international conventions and funding mechanisms; using conservation biology to build a better understanding of zoonotic diseases; more effectively addressing human–animal conflicts; enhancing community-based conservation; and using conservation biology to help address the pervasive water-deficit problems in much of Asia. These challenges can be met through improved regional cooperation among the relevant stakeholders .     

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.     

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.     

Conservation genomics of the endangered Burmese roofed turtle

The Burmese roofed turtle (Batagur trivittata) is one of the world's most endangered turtles. Only one wild population remains in Myanmar. There are thought to be 12 breeding turtles in the wild. Conservation efforts for the species have raised >700 captive turtles since 2002, predominantly from eggs collected in the wild. We collected tissue samples from 445 individuals (approximately 40% of the turtles’ remaining global population), applied double‐digest restriction‐site associated DNA sequencing (ddRAD‐Seq), and obtained approximately 1500 unlinked genome‐wide single nucleotide polymorphisms. Individuals fell into 5 distinct genetic clusters, 4 of which represented full‐sib families. We inferred a low effective population size (≤10 individuals) but did not detect signs of severe inbreeding, possibly because the population bottleneck occurred recently. Two groups of 30 individuals from the captive pool that were the most genetically diverse were reintroduced to the wild, leading to an increase in the number of fertile eggs (n = 27) in the wild. Another 25 individuals, selected based on the same criteria, were transferred to the Singapore Zoo as an assurance colony. Our study demonstrates that the research‐to‐application gap in conservation can be bridged through application of cutting‐edge genomic methods.     

Limitations of Captive Breeding in Endangered Species Recovery

The use of captive breeding in species recovery has grown enormously in recent years, but without a concurrent growth in appreciation of its limitations. Problems with (1) establishing self-sufficient captive populations, (2) poor success in reintroductions, (3) high costs, (4) domestication, (5) preemption of other recovery techniques, (6) disease outbreaks, and (7) maintaining administrative continuity have all been significant. The technique has often been invoked prematurely and should not normally be employed before a careful field evaluation of costs and benefits of all conservation alternatives has been accomplished and a determination made that captive breeding is essential for species survival. Merely demonstrating that a species' population is declining or has fallen below what may be a minimum viable size does not constitute enough analysis to justify captive breeding as a recovery measure. Captive breeding should be viewed as a last resort in species recovery and not a prophylactic or long-term solution because of the inexorable genetic and phenotypic changes that occur in captive environments. Captive breeding can play a crucial role in recovery of some species for which effective alternatives are unavailable in the short term. However, it should not displace habitat and ecosystem protection nor should it be invoked in the absence of comprehensive efforts to maintain or restore populations in wild habitats. Zoological institutions with captive breeding programs should operate under carefully defined conditions of disease prevention and genetic/behavioral management. More important, these institutions should help preserve biodiversity through their capacities for public education, professional training, research, and support of in situ conservation efforts.     

Application of Reproduction Technologies to the Conservation of Genetic Resources

Abstract: Maintaining the levels of genetic variability in captive populations of endangered species is an important objective of conservation biology. Because of the generally low sizes of captive populations, genetic drift is the main cause of loss of diversity. Several simple management rules, such as equalization of contributions from parents to the next generation, are recommended for minimizing genetic drift, but it cannot be removed completely because of the unavoidable random segregation of heterozygotes. Recent advances in reproductive technology, particularly developed for mammals, are now making a reality of the possibility of using more than one cell from a single meiosis in reproduction. With this technology it is possible to reduce or even completely cancel the genetic drift caused by segregation of heterozygotes. We evaluated the theoretical benefits of the use of such technologies to conservation biology. The effective population size can be increased enormously and, consequently, the amount of drift can be greatly reduced if manipulations in reproduction are made.     

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.     

Consensus versus Conservation in the Upper Colorado River Basin Recovery Implementation Program

Abstract: We examined consensus-based management through the lens of the Colorado River Recovery Implementation Program, a consensus-based plan that attempts to develop the Colorado River's water while protecting its endangered fishes. Because this management model has been touted as a preferred substitute to government-imposed regulation, we analyzed the recovery implementation program to determine its strengths and weaknesses. By reviewing secondary information and interviewing members of the diverse groups involved in the program, we gathered detailed information about the program's history, implementation, and progress. Our investigation revealed that the recovery implementation program has allowed development of the Colorado River's water and incorporated more voices into the decision-making process. But the program circumvented federal authority over endangered species conservation, which has proved detrimental to the fishes. Furthermore, we learned that the consensus-based model is vulnerable to control by special-interests and may be driven by bureaucratic procedural goals rather than species recovery. To ameliorate these concerns, (1) program success should be judged by species recovery, rather than political achievements, (2) the federal government should retain the power of issuing statutory sanctions in the event of continued population decline, and (3) funding should be provided by an agency with a clear species-protection agenda to reduce the disproportionate power of utilitarian interest groups. By incorporating these recommendations, conservation programs can better realize the benefits of a consensus-based approach without sacrificing species recovery.     

Limits to captive breeding of mammals in zoos

Captive breeding of mammals in zoos is the last hope for many of the best‐known endangered species and has succeeded in saving some from certain extinction. However, the number of managed species selected is relatively small and focused on large‐bodied, charismatic mammals that are not necessarily under strong threat and not always good candidates for reintroduction into the wild. Two interrelated and more fundamental questions go unanswered: have the major breeding programs succeeded at the basic level of maintaining and expanding populations, and is there room to expand them? I used published counts of births and deaths from 1970 to 2011 to quantify rates of growth of 118 captive‐bred mammalian populations. These rates did not vary with body mass, contrary to strong predictions made in the ecological literature. Most of the larger managed mammalian populations expanded consistently and very few programs failed. However, growth rates have declined dramatically. The decline was predicted by changes in the ratio of the number of individuals within programs to the number of mammal populations held in major zoos. Rates decreased as the ratio of individuals in programs to populations increased. In other words, most of the programs that could exist already do exist. It therefore appears that debates over the general need for captive‐breeding programs and the best selection of species are moot. Only a concerted effort could create room to manage a substantially larger number of endangered mammals. Los Límites para la Reproducción en Cautiverio de Mamíferos en Zoológicos Alroy     

Use of Substitute Species in Conservation Biology

Abstract:  In conservation biology, researchers often want to study the reasons why an endangered population is faring poorly but are unable to study it directly for logistical or political reasons. Instead they study a species that substitutes for the one of concern in the hope that it will cast light on the conservation problem. Here we outline the assumptions underlying this approach. Substitutes can be different populations or species and may be chosen because they are similar biologically to the target or representatives of a constellation of species of which the target is one. They also may be used to develop a predictive model to which the conservation target can be related. For substitutes to be appropriate, they should share the same key ecological or behavioral traits that make the target sensitive to environmental disturbance and the relationship between population vital rates and level of disturbance should match that of the target. These conditions are unlikely to pertain in most circumstances and the use of substitute species to predict endangered populations' responses to disturbance is questionable.     

Inbreeding Depression in the Speke's Gazelle Captive Breeding Program

Abstract: The Speke's gazelle ( Gazella spekei ) captive breeding program has been presented as one of the few examples of selection reducing the genetic load of a population and as a potential model for the captive breeding of endangered species founded from a small number of individuals. In this breeding program, three generations of mate selection apparently increased the viability of inbred individuals. We reanalyzed the Speke's gazelle studbook and examined potential causes for the reduction of inbreeding depression. Our analysis indicates that the decrease in inbreeding depression is not consistent with any model of genetic improvement in the herd. Instead, we found that the effect of inbreeding decreased from severe to moderate during the first generation of inbreeding, and that this change is responsible for almost all of the decline in inbreeding depression observed during the breeding program. This eliminates selection as a potential explanation for the decrease in inbreeding depression and suggests that inbreeding depression may be more sensitive to environmental influences than is usually thought.     

Diagnosing Units of Conservation Management

Species-oriented conservation programs attempt to analyze and maintain intra-specific variation in order to maximally preserve biological diversity. The "evolutionarily significant unit" has become an operational term for a group of organisms that should be the minimial unit for conservation management. No generally accepted definition for this term exists that would be the basis for the evaluation of these units in practical conservation situations. Currently, taxonomic decisions in species conservation are mostly based on the biological species concept. But the universal application of criteria of reproductive isolation or phenetic similarity to delimit conservation units is problematical. We favor a definition for evolutionarily significant units based on patterns of variation. In the theoretical framework of the phylogenetic species concept, conservation units are delimited by characters that diagnose clusters of individuals or populations to the exclusion of other such clusters. Characters are used for cladistic analysis to infer hypotheses of the phylogenetic relationships of individuals, and differentiated populations are diagnosed using population aggregation analysis. Characters can be based on genetic, morphological, ecological, or behavioral information, provided they are inferred to be heritable. The use of cladistics and population aggregation analysis has the potential to make the evaluation of evoluntionarily significant units objective and testable, an important consideration in politically controversial cases. Our cladistic approach is demonstrated by the evaluation of potential conservation units in the endangered tiger beetles Cicindela dorsalis and C. puritana .     

Genetically informed captive breeding of hybrids of an extinct species of Galapagos tortoise

Hybridization poses a major challenge for species conservation because it threatens both genetic integrity and adaptive potential. Yet, hybridization can occasionally offer unprecedented opportunity for species recovery if the genome of an extinct taxon is present among living hybrids such that selective breeding could recapture it. We explored the design elements for establishing a captive-breeding program for Galapagos tortoises (Chelonoidis spp.) built around individuals with admixed ancestry involving an extinct species. The target individuals were hybrids between the extinct species from Floreana Island, C. niger, and an extant species, C. becki, which were recently found in the endemic range of C. becki, from Wolf Volcano on Isabela Island. We combined genotypic data from 35 tortoises with high ancestry from C. niger with forward-in-time simulations to explore captive breeding strategies that maximized overall genetic diversity and ancestry from C. niger while accommodating resource constraints, species biology, and the urgency to return tortoises to Floreana Island for facilitating ecosystem restoration. Overall genetic diversity was maximized when in the simulation tortoises were organized in relatively small breeding groups. Substantial amounts of the C. niger genome were captured despite limited resources available for selectively breeding tortoises in captivity. Genetic diversity was maximized when captive-bred offspring were released to the wild rather than being used as additional breeders. Our results provide genetic-based and practical guidance on the inclusion of hybrids with genomic representation from extinct taxa into species restoration programs and informs the ongoing debate on the value of hybrids in biodiversity conservation.