Conservation genomics of desert dwelling California voles (<Emphasis Type="Italic">Microtus californicus</Emphasis>) and implications for management of endangered Amargosa voles (<Emphasis Type="Italic">Microtus californicus scirpensis</Emphasis>)

Understanding population genetic structure and levels of genetic variation is critical for the conservation and management of imperiled populations, especially when reintroductions are planned. We used restriction-site associated DNA (RAD) sequencing to study the genetic diversity and evolutionary relationships of the endangered Amargosa vole and other closely related desert-dwelling California voles. Specifically, we sought to determine how Amargosa voles are related to other California voles, how genetic variation is partitioned among subpopulations in wild Amargosa voles, and how much genetic variation is captured within a captive insurance colony of Amargosa voles. Our multilocus nuclear dataset provides strong evidence that Amargosa voles are part of a northern clade of California voles. Amargosa voles have highly reduced genetic variation relative to other California voles, but do exhibit some sub-structure among sampled marshes. Captive Amargosa voles capture approximately half of the total genetic variation present in the wild Amargosa vole populations. We discuss the management implications of our findings in light of reintroductions planned for Amargosa voles. Our study highlights the utility of reduced representation genomic approaches, like RADseq, to resolve relationships among small populations that are difficult to study with traditional markers due to low genetic variation and few individuals left in the wild.     

Genetic rescue of an inbred captive population of the critically endangered Puerto Rican crested toad (<Emphasis Type="Italic">Peltophryne lemur</Emphasis>) by mixing lineages

The Puerto Rican crested toad (Peltophryne lemur) is currently composed of a single wild population on the south coast of Puerto Rico and two captive populations founded by animals from the northern and southern coasts. The main factors contributing to its decline are habitat loss, inundation of breeding ponds during storms, and impacts of invasive species. Recovery efforts have been extensive, involving captive breeding and reintroductions, habitat restoration, construction of breeding ponds, and public education. To guide future conservation efforts, genetic variation and differentiation were assessed for the two captive colonies and the remaining wild population using the mitochondrial control region and six novel microsatellite loci. Only two moderately divergent mitochondrial haplotypes were found, with one fixed in each of the southern and northern lineages. Moderate genetic variation exists for microsatellite loci in all three groups. The captive southern population has not diverged substantially from the wild population at microsatellite loci (F _ST = 0.03), whereas there is little allelic overlap between the northern and southern lineages at five of six loci (F _ST > 0.3). Despite this differentiation, they are no more divergent than many populations of other amphibian species. As the northern breeding colony may not remain viable due to its small size and inbred nature, it is recommended that a third breeding colony be established in which northern and southern individuals are combined. This will preserve any northern adaptive traits that may exist, and provide animals for release in the event that the pure northern lineage becomes extirpated.     

Breeding program for the lesser kudu (Tragelaphus imberbis) in North America

The lesser kudu (Tragelaphus imberbis) has been kept in North American zoological parks since 1930 but has never been a common species in collections. In 1987 this population totaled 28 animals: 15 males and 13 females. A pedigree evaluation in 1987 of the existing population indicated that eight effective founders and one potential founder were represented in the North American herd. Three new potential founders from European captive populations were added to the population in 1987 to increase the number of existing founder lines to 12 animals. As this species is not endangered or threatened in its native habitat, it is not a high priority to qualify for designation as an SSP species. Because of this, the institutions holding lesser kudu in North America decided to join informally and draft a breeding program to better manage this small captive population. This program was designed to minimize inbreeding and equalize genetic representation of founder animals to maximize genetic diversity. It requires a shift in management philosophy to establish stable groups of breeding females at participating institutions while rotating appropriate breeder males through these herds in a controlled manner to ensure minimization of inbreeding and maximization of genetic diversity. It is hoped that this program can serve as a model for the management of other small captive populations of non-SSP species.     

Putting the Spotlight on Internally Displaced Animals (IDAs): A Survey of Primate Sanctuaries in Africa,Asia, and the Americas

As anthropogenic activity makes deeper incursions into forests, fragmenting habitat, wildlife is forced into closer proximity to humans leading to increased incidences of human–wildlife conflict and wildlife displacement. These same incursions facilitate poaching for the commercial trade in dead and live animals. As a direct result, the number of sanctuaries and internally displaced animals (IDAs) in need of sanctuary placement and rehabilitation are increasing. We focus on internally displaced primates given the prevalence of primate‐focused facilities and anthropomorphic considerations surrounding this taxonomic group. Surveys were distributed globally to map the extent and range of native primate sanctuaries and species. Over 70 facilities care for more than 6,000 native primates comprising 64 species, with almost half listed as endangered or critically endangered. As not all sanctuaries were identified at the time of the survey distribution, we estimate that the actual number of facilities is closer to double this number with a captive population in excess of 10,000 individual primates. Native primate sanctuaries hold significant numbers of primates in long‐term captive care, with less than half (37%) identified as candidates for release. The surveyed sanctuary population accounts for 35% of the world's captive primates, as compared to ISIS‐registered (where ISIS is International Species Information System) zoological facilities, although we estimate that the actual population is closer to 58%. For some species, the sanctuary population represents the only population in captivity. We discuss the prevalence of range‐state sanctuaries and their primate populations, and issues surrounding their future development and management. Am. J. Primatol. 75:116‐134, 2013. © 2012 Wiley Periodicals, Inc.     

Successful breeding attempt of a pair of Philippine tarsier (Tarsius syrichta) in a conservation center in Bilar,Bohol, Philippines and recommendations for tarsier husbandry

The Philippine tarsier (Tarsius syrichta) belongs to the least known nocturnal primates. Tarsiers and remaining biodiversity of the Philippines are under tremendous threats from increasing human expansion, with habitat loss and illegal pet trade being the main reasons for tarsier population decline. In addition, even though the attempts were made by western and local facilities, tarsiers have not survived well in captivity. In this paper, I present an example of successful breeding of the Philippine tarsier in captive conditions but in natural climate. As the most important elements of success, I see a large amount of space provided to tarsiers, the climate similar to their natural habitat and the food resembling their natural diet. Our pair of tarsiers were joined during the mating period and held separately outside the mating period, which corresponds with their behavior in the wild and may have played a crucial role in breeding success. Eliminating stress to animals is also important. The study can provide valuable guidelines for other facilities keeping tarsiers in the Philippines and help to improve tarsiers’ welfare and in the future help to establish a viable captive population of the Philippine tarsier that will serve as a backup population and also will decrease demand on tarsiers captured from the wild.     

The pronghorn (Antilocapra americana): A review as a model for development of a “Species Management Plan” format,Part I

A format is suggested for a “Species Management Plan”; the model for this presentation is the pronghorn (Antilocapra americana). By using the Species Management Plan format, the captive maintenance of pronghorn is analyzed in relation to habitat and microhabitat needs, behavioral requirements, and nutritional needs. A strategy for captive maintenance of pronghorn in relatively wet climates is presented. It is suggested that development of a Species Management Plan is necessary before any new species is acquired for captive maintenance and reproduction.     

Unique multiple paternity in the endangered big‐headed turtle (Platysternon megacephalum) in an ex situ population in South China

Understanding the mating system and reproductive strategies of an endangered species is critical to the success of captive breeding. The big‐headed turtle (Platysternon megacephalum) is one of the most threatened turtle species in the world. Captive breeding and reintroduction are necessary to re‐establish wild populations of P. megacephalum in some of its historical ranges in China, where the original populations have been extirpated. However, the captive breeding of P. megacephalum is very difficult and this may be due to its mysterious reproductive strategies and special behavior (e.g., aggressive temperament and territoriality). In this study, we achieved successful captive breeding of P. megacephalum by creating a habitat that mimics natural conditions and then investigated its mating system using microsatellite makers. A total of 16 clutches containing 79 eggs of P. megacephalum were collected, and 52 were hatched successfully over two breeding seasons. Of the 15 effective clutches, 6 clutches (40%) exhibited multiple paternity. There was no significant correlation between clutch size and multiple paternity, and no significant difference in hatching success between multiple‐sired and single‐sired clutches. However, there was significant correlation between male body size and the number of offspring, with higher‐ranked males contributing to more clutches. Our results provide the first evidence of multiple paternity and male hierarchy in P. megacephalum. These findings suggest that multiple paternity and male hierarchy should be considered in captive breeding programs for P. megacephalum, and creating a habitat that mimics natural conditions is an effctive way to achieve successful captive breeding and investigate the mating systems of this species.     

Parentage verification of a mountain zebra (Equus zebra hartmannae) using polymorphic microsatellite markers

The Hartmann's mountain zebra (Equus zebra hartmannae) has been classified by the IUCN as a vulnerable species. Approximately 300 individuals, maintained in zoos throughout Europe and the United States of America, are being managed as part of a captive breeding program. An International Studbook is maintained for the Hartmann's mountain zebra at Marwell Zoological Park, UK. Despite the use of a variety of means to identify each individual in a captive herd, confusion sometimes occurs, resulting in the misidentification of an animal. Here we report the first application of DNA typing, using polymorphic microsatellite loci, to resolve a misidentification involving two female Hartmann's mountain zebra. This case demonstrates the way in which genetic tests derived from a related domesticated species may be used as an effective tool for captive management. Further, this case highlights the need to be able to conclusively identify captive individuals and to maintain accurate pedigree information for successful captive management. © 1995 Wiley-Liss, Inc.     

Population Genetics of the Washington National Primate Research Center's (WaNPRC) Captive Pigtailed Macaque (Macaca nemestrina) Population

Pigtailed macaques (Macaca nemestrina) provide an important model for biomedical research on human disease and for studying the evolution of primate behavior. The genetic structure of captive populations of pigtailed macaques is not as well described as that of captive rhesus (M. mulatta) or cynomolgus (M. fascicularis) macaques. The Washington National Primate Research Center houses the largest captive colony of pigtailed macaques located in several different housing facilities. Based on genotypes of 18 microsatellite (short tandem repeat [STR]) loci, these pigtailed macaques are more genetically diverse than captive rhesus macaques and exhibit relatively low levels of inbreeding. Colony genetic management facilitates the maintenance of genetic variability without compromising production goals of a breeding facility. The periodic introduction of new founders from specific sources to separate housing facilities at different times influenced the colony's genetic structure over time and space markedly but did not alter its genetic diversity significantly. Changes in genetic structure over time were predominantly due to the inclusion of animals from the Yerkes National Primate Research Center in the original colony and after 2005. Strategies to equalize founder representation in the colony have maximized the representation of the founders’ genomes in the extant population. Were exchange of animals among the facilities increased, further differentiation could be avoided. The use of highly differentiated animals may confound interpretations of phenotypic differences due to the inflation of the genetic contribution to phenotypic variance of heritable traits. Am. J. Primatol. 74:1017‐1027, 2012. © 2012 Wiley Periodicals, Inc.     

Modeling problems in conservation genetics using captive Drosophila populations: Rapid genetic adaptation to captivity

Long-term captive breeding programs for endangered species generally aim to preserve the option of release back into the wild. However, the success of re-release programs will be jeopardized if there is significant genetic adaptation to the captive environment. Since it is difficult to study this problem in rare and endangered species, a convenient laboratory animal model is required. The reproductive fitness of a large population of Drosophila melanogaster maintained in captivity for 12 months was compared with that of a recently caught wild population from the same locality. The competitive index measure of reproductive fitness for the captive population was twice that of the recently caught wild population, the difference being highly significant. Natural selection over approximately eight generations in captivity has caused rapid genetic adaptation. Captive breeding strategies for endangered species should minimize adaptation to captivity in populations destined for reintroduction into the wild. A framework for predicting the impact of factors on the rate of genetic adaptation to captivity is suggested. Equalization of family sizes is predicted to approximately halve the rate of genetic adaptation. Introduction of genes from the wild, increasing the generation interval, using captive environments close to those in the wild and achieving low mortality rates are all expected to slow genetic adaptation to captivity. Many of these procedures are already recommended for other reasons. © 1992 Wiley-Liss, Inc.     

The current status and future prospects of the Red Panda (Ailurus fulgens) studbook population

Scientifically based captive breeding programs are an essential prerequisite to the long-term preservation of exotic species in zoos. The data provided by studbooks form the foundation on which such a program can be built. In the following paper, information extracted from the International Studbook for the Red Panda (Ailurus fulgens) is used to provide both demographic and genetic analyses of the current captive-born population and simulations of future trends in population structure. From the results of these analyses, conclusions can be drawn which are of importance to future captive management practice.     

Survival rates of captive‐bred Asian Houbara Chlamydotis macqueenii in a hunted migratory population

Asian Houbara Chlamydotis macqueenii numbers are declining as a result of unsustainable levels of hunting and poaching, with the main conservation response being population reinforcement through the release of captive‐bred birds. We assessed the contribution of captive breeding to the species’ conservation by examining the fates of 65 captive‐bred birds fitted with satellite transmitters and released during spring (March–May) and autumn (August) into breeding habitat in Uzbekistan. Of the released birds, 58.5% survived to October, the month favoured by Emirati hunters in Uzbekistan, but only 10.8% of those released survived the winter to return as subadults next spring. To mitigate and compensate for the loss of wild adults to hunting, the number of released birds needs to be an order of magnitude higher than hunting quotas (with a release of between 1640 and 1920 required for a hypothetical quota of 200), indicating that releases may be costly and do not remove the need for a biologically determined sustainable hunting quota.     

Captive breeding of pangolins: current status,problems and future prospects

Pangolins are unique placental mammals with eight species existing in the world, which have adapted to a highly specialized diet of ants and termites, and are of significance in the control of forest termite disaster. Besides their ecological value, pangolins are extremely important economic animals with the value as medicine and food. At present, illegal hunting and habitat destruction have drastically decreased the wild population of pangolins, pushing them to the edge of extinction. Captive breeding is an important way to protect these species, but because of pangolin’s specialized behaviors and high dependence on natural ecosystem, there still exist many technical barriers to successful captive breeding programs. In this paper, based on the literatures and our practical experience, we reviewed the status and existing problems in captive breeding of pangolins, including four aspects, the naturalistic habitat, dietary husbandry, reproduction and disease control. Some recommendations are presented for effective captive breeding and protection of pangolins.     

Seasonal behavioral patterns of captive alpine musk deer (<Emphasis Type="Italic">Moschus sifanicus</Emphasis>): Rut and pre-rut comparisons

Alpine musk deer (Moschus sifanicus), well-known for their musk production, are endemic to western China. Due to historical unrestricted illegal hunting and habitat loss, captive farming has been employed as a means of conserving this endangered species and developing sustainable musk harvesting techniques. For captive animals, an understanding of behavioral characteristics is vital to improve management practices. This study addressed a lack of information regarding the behavioral characteristics of alpine musk deer; specifically daily activity patterns in respect to gender and reproductive season. From August 2002 to January 2003, focal sampling was employed to observe 32 adult captive alpine musk deer (13 females and 19 males), at Xinglongshan Musk Deer Farm (XMDF), located at Xinglongshan National Nature Reserve, Gansu Province, China. Results indicated that the general behavioral patterns were similar between female and male captive alpine musk deer throughout both reproductive and non-reproductive seasons (rut and pre-rut season). Both male and female alpine musk deer demonstrated tail-pasting behavior during rut season, a previously male-only behavior trait. Female musk deer also rested comparatively more than males during pre-rut season.     

Skeletal development in Pan paniscus with comparisons to Pan troglodytes

Fusion of skeletal elements provides markers for timing of growth and is one component of a chimpanzee's physical development. Epiphyseal closure defines bone growth and signals a mature skeleton. Most of what we know about timing of development in chimpanzees derives from dental studies on Pan troglodytes. Much less is known about the sister species, Pan paniscus, with few in captivity and a wild range restricted to central Africa. Here, we report on the timing of skeletal fusion for female captive P. paniscus (n = 5) whose known ages range from 0.83 to age 11.68 years. Observations on the skeletons were made after the individuals were dissected and bones cleaned. Comparisons with 10 female captive P. troglodytes confirm a generally uniform pattern in the sequence of skeletal fusion in the two captive species. We also compared the P. paniscus to a sample of three unknown‐aged female wild P. paniscus, and 10 female wild P. troglodytes of known age from the Taï National Park, Côte d'Ivoire. The sequence of teeth emergence to bone fusion is generally consistent between the two species, with slight variations in late juvenile and subadult stages. The direct‐age comparisons show that skeletal growth in captive P. paniscus is accelerated compared with both captive and wild P. troglodytes populations. The skeletal data combined with dental stages have implications for estimating the life stage of immature skeletal materials of wild P. paniscus and for more broadly comparing the skeletal growth rates among captive and wild chimpanzees (Pan), Homo sapiens, and fossil hominins. Am J Phys Anthropol 2012. © 2012 Wiley Periodicals, Inc.     

Reproductive Parameters of Female<Emphasis Type="Italic">Pan paniscus</Emphasis> and <Emphasis Type="Italic">P. troglodytes</Emphasis>: Quality versus Quantity

We investigated intra- and interspecific differences in life history and reproductive parameters in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We compare the parameters of wild and captive females in order to shed light on the influence of habitat or specific differences or both on reproduction. We present new and additional information on reproductive parameters from captive bonobos and chimpanzees. Captive chimpanzees birth more live offspring and have a shorter interbirth interval, but experience higher infant mortality than captive bonobos. Although captive bonobo females tend to start reproduction at a younger age than chimpanzees, this is effectively only so for wild-born females of both species. Ultimately both species reach the same rate of production of offspring surviving to 5 yr. These results contrast with data from the wild. Wild bonobos tend to have higher reproductive success, a higher fertility rate and a shorter interbirth interval than wild chimpanzees. Reproduction is similar for wild and captive bonobos, which suggests that they are producing at their maximum under both conditions. Overall captive chimpanzees perform better than their wild conspecifics, probably because of lower feeding competition. Infant survival is the only specific difference not affected by captivity. Bonobo infants survive better, which suggests that chimpanzee infants are more at risk. We argue that the interspecific variation in reproductive parameters in captivity is related to the different influence of captivity on reproduction and different pressures of external sources of infant and juvenile mortality.     

Reproductive behavior of the captive Sunda pangolin (Manis javanica Desmarest, 1822)

Understanding reproductive behavior is important for the conservation of endangered species, but research on the reproductive behavior of Sunda pangolins (Manis javanica Desmarest, 1822) is still very scarce. In this study, we used focal animal sampling and all-occurrence recording by an infrared monitor to observe the behaviors of two Sunda pangolins during a 5-day breeding period at the Pangolin Research Base for Artificial Rescue and Conservation Breeding of South China Normal University (PRB-SCNU). The behavioral characteristics and breeding strategies were analyzed, and the results were discussed together with information on other captive Sunda pangolin pairs at PRB-SCNU. The results found that there was no obvious estrus behavior in the captive female, while the male could exhibit sexual excitement and courtship behavior after a brief introduction period. Repeated copulation continued over many days after the female accepted the courtship. The average duration of copulatory behavior was 248.9 ± 148.7 s (n = 25), and all copulation occurred between 20:00 and 08:00 hr in the natural day–night photoperiod. The mating position of Sunda pangolins was lateral–ventral and was classified as the ninth or eleventh pattern under both Dewsbury's and Dixson's classification systems. This study can provide scientific guidance for the captive breeding and management of Sunda pangolins and other pangolin species, which is of great significance for ex situ conservation tactics.     

Blood values of Bald Ibis ( Geronticus eremita) in captivity: comparative ranges and variability with age, sex and physical condition

The Bald Ibis (Geronticus eremita) is one of the worlds most threatened species of birds. The number of individuals in captivity is several times greater than the number of individuals in the wild, so that the re-introduction of individuals from captive breeding into their natural habitat may be vital for the recovery of the species. A knowledge of the health problems associated with the handling of captive individuals and the improvement of their veterinary care could have great importance in determining the success of these captive breeding programs. Haematology and blood chemistry are very useful complementary tools in the diagnosis and treatment of diseases in birds, and provide valuable information about the individuals nutritional status and physical condition. The present work reports haematocrit and blood chemistry values for individuals belonging to a captive population of this species, and analyses their variability with respect to age, sex, and physical condition of the animals. Adults presented greater values of haematocrit, uric acid, total proteins, cholesterol, and aspartate amine transferase than the young. With respect to sex differences, adult female birds had higher concentrations of alkaline phosphatase than males, contrary to previous results for captive individuals of this species. The condition index of adults was positively correlated with triglycerides, glucose, and alkaline phosphatase levels, and negatively with urea and lactate dehydrogenase levels. These results may be very useful as a complementary diagnosis tool during the veterinary care of individuals of this species included in re-introduction programs.     

Captive care and welfare considerations for beavers

Beavers (Castor spp.) tend not to be a commonly held species and little published material exists relating to their captive care. We review published material and discuss husbandry issues taking into account the requirements of wild beavers. As social mammals with complex chemical communication systems and with such an ability to modify their environments, studies of wild counterparts suggest the captive requirements of beavers may actually be more sophisticated than generally perceived. Common field techniques may have practical application in the captive setting. Their widespread utilisation in conservation, including reintroductions, translocations and habitat management, also requires components of captive care. As welfare science advances there is increasing pressure on captive collections to improve standards and justify the keeping of animals. Conservation science is increasingly challenged to address individual welfare standards. Further research focusing on the captive care of beavers is required. Zoo Biol. 34:101–109, 2015. © 2015 The Authors. Zoo Biology published by Wiley Periodicals, Inc.     

An Ixodes minor and Borrelia carolinensis enzootic cycle involving a critically endangered Mojave Desert rodent

Microtus californicus scirpensis is an endangered, isolated subspecies of California vole. It requires water pools and riparian bulrush (Schoenoplectus americanus) and occupies some of the rarest habitat of any North American mammal. The minimally vegetated, extremely arid desert surrounding the pools is essentially uninhabitable for Ixodes species ticks. We describe an enzootic cycle of Borrelia carolinensis in Ixodes minor ticks at a site 3500 km distant from the region in which I. minor is known to occur in Tecopa Host Springs, Inyo County, eastern Mojave Desert, California. Voles were live‐trapped, and ticks and blood samples queried by PCR and DNA sequencing for identification and determination of the presence of Borrelia spp. Between 2011–2013, we found 21 Ixodes minor ticks (prevalence 4–8%) on Amargosa voles and Reithrodontomys megalotis. DNA sequencing of 16S rRNA from ticks yielded 99% identity to I. minor. There was 92% identity with I. minor in the calreticulin gene fragment. Three ticks (23.1%), 15 (24%) voles, three (27%) house mice, and one (7%) harvest mice were PCR positive for Borrelia spp. Sequencing of the 5S‐23S intergenic spacer region and flagellin gene assigned Amargosa vole Borrelia strains to B. carolinensis. Ixodes minor, first described in 1902 from a single Guatemalan record, reportedly occurs only in the southeast American on small mammals and birds. The source of this tick in the Mojave Desert and time scale for introduction is not known but likely via migratory birds. Borrelia strains in the Amargosa ecosystem most closely resemble B. carolinensis. B. carolinensis occurs in a rodent‐I. minor enzootic cycle in the southeast U.S. although its epidemiological significance for people or rodents is unknown. The presence of a tick and Borrelia spp. only known from southeast U.S. in this extremely isolated habitat on the other side of the continent is of serious concern because it suggests that the animals in the ecosystem could be vulnerable to further incursions of pathogens and parasites.