• A comparison of strategies for selecting breeding pairs to maximize genetic diversity retention in managed populations

      Ivy, Jamie A.; Lacy, Robert C. (2012)
      Captive breeding programs aim to maintain populations that are demographically self-sustaining and genetically healthy. It has been well documented that the best way for managed breeding programs to retain gene diversity (GD) and limit inbreeding is to select breeding pairs that minimize a population's average kinship....
    • A demonstration of conservation genomics for threatened species management

      Wright, Belinda R.; Farquharson, Katherine A.; McLennan, Elspeth A.; Belov, Katherine; Hogg, Carolyn J.; Grueber, Catherine E. (2020)
      ... We conducted whole genome sequencing (WGS) of 25 individuals from the captive breeding programme and reduced‐representation sequencing (RRS) of 98 founders of the same programme. A subset of the WGS samples was also sequenced by RRS, allowing us to directly compare genome‐wide heterozygosity with estimates from RRS data. We found good congruence in interindividual variation and gene‐ontology classifications between the two data sets, indicating that our RRS data reflect the genome well....
    • A meta-analysis of birth-origin effects on reproduction in diverse captive environments

      Farquharson, Katherine A.; Hogg, Carolyn J.; Grueber, Catherine E. (2018)
      Successfully establishing captive breeding programs is a priority across diverse industries to address food security, demand for ethical laboratory research animals, and prevent extinction. Differences in reproductive success due to birth origin may threaten the long-term sustainability of captive breeding. Our meta-analysis examining 115 effect sizes from 44 species of invertebrates, fish, birds, and mammals shows that, overall, captive-born animals have a 42% decreased odds of reproductive success in captivity compared to their wild-born counterparts. The largest effects are seen in commercial aquaculture, relative to conservation or laboratory settings, and offspring survival and offspring quality were the most sensitive traits. Although a somewhat weaker trend, reproductive success in conservation and laboratory research breeding programs is also in a negative direction for captive-born animals. Our study provides the foundation for future investigation of non-genetic and genetic drivers of change in captivity, and reveals areas for the urgent improvement of captive breeding.
    • A suite of microsatellite markers optimized for amplification of DNA from addax (Addax nasomaculatus) blood preserved on FTA cards: Microsatellites for addax on FTA cards

      Heim, Brett C.; Ivy, Jamie A.; Latch, Emily K. (2012)
      The addax (Addax nasomaculatus) is a critically endangered antelope that is currently maintained in zoos through regional, conservation breeding programs. As for many captive species, incomplete pedigree data currently impedes the ability of addax breeding programs to confidently manage the genetics of captive populations and to select appropriate animals for reintroduction. Molecular markers are often used to improve pedigree resolution, thereby improving the long‐term effectiveness of genetic management....
    • Activation of southern white rhinoceros (Ceratotherium simum simum) estrogen receptors by phytoestrogens: Potential role in the reproductive failure of captive-born females?

      Tubbs, Christopher W.; Hartig, P.; Cardon, M.; Varga, Nicole; Milnes, Matthew R. (2012)
      The captive southern white rhinoceros (SWR; Ceratotherium simum simum) population serves as an important genetic reservoir critical to the conservation of this vulnerable species. Unfortunately, captive populations are declining due to the poor reproductive success of captive-born females....
    • Alsophis sibonius (NCN) copulation

      Knapp, Charles R.; Shirk, P.L.; (2010)
      Alsophis sibonius is a diurnal, actively foraging snake inhabiting the Commonwealth of Dominica, West Indies....Here we report a field observation of copulation for A. sibonius from the Caribbean side of Dominica....
    • Animal Welfare in Conservation Breeding: Applications and Challenges

      Greggor, Alison L.; Vicino, Greg A.; Swaisgood, Ronald R.; Fidgett, Andrea; Brenner, Deena J.; Kinney, Matthew E.; Farabaugh, Susan M.; Masuda, Bryce M.; Lamberski, Nadine (2018)
      Animal welfare and conservation breeding have overlapping and compatible goals that are occasionally divergent. Efforts to improve enclosures, provide enriching experiences, and address behavioral and physical needs further the causes of animal welfare in all zoo settings. However, by mitigating stress, increasing behavioral competence, and enhancing reproduction, health, and survival, conservation breeding programs must also focus on preparing animals for release into the wild. Therefore conservation breeding facilities must strike a balance of promoting high welfare, while minimizing the effects of captivity to increase population sustainability. As part of the Hawaii Endangered Bird Conservation Program, San Diego Zoo Global operates two captive breeding facilities that house a number of endangered Hawaiian bird species. At our facilities we aim to increase captive animal welfare through husbandry, nutrition, behavior-based enrichment, and integrated veterinary practices. These efforts help foster a captive environment that promotes the development of species-typical behaviors. By using the “Opportunities to Thrive” guiding principles, we outline an outcome-based welfare strategy, and detail some of the related management inputs, such as transitioning to parental rearing, and conducting veterinary exams remotely. Throughout we highlight our evidence-based approach for evaluating our practices, by monitoring welfare and the effectiveness of our inputs. Additionally we focus on some of the unique challenges associated with improving welfare in conservation breeding facilitates and outline concrete future steps for improving and evaluating welfare outcomes that also meet conservation goals.
    • Appendix 4: Annotated bibliography of books, journals, and web sites on captive management.

      Kenyon Barboza, K.; Coates, Linda L.; Kleiman, Devra G. (University of Chicago Press, 2010)
      ...Wild Mammals in Captivity presents the most current thinking and practice in the care and management of wild mammals in zoos and other institutions. In one comprehensive volume, the editors have gathered the most current information from studies of animal behavior; advances in captive breeding; research in physiology, genetics, and nutrition; and new thinking in animal management and welfare.....
    • Applying SNP-derived molecular coancestry estimates to captive breeding programs

      Ivy, Jamie A.; Putnam, Andrea S.; Navarro, Asako Y.; Gurr, Jessica; Ryder, Oliver A. (2016)
      ...Although pedigree-based breeding strategies are quite effective at retaining long-term genetic variation, management of zoo-based breeding programs continues to be hampered when pedigrees are poorly known. The objective of this study was to evaluate 2 options for generating single nucleotide polymorphism (SNP) data to resolve unknown relationships within captive breeding programs...
    • Are any populations ‘safe’? Unexpected reproductive decline in a population of Tasmanian devils free of devil facial tumour disease

      Farquharson, Katherine A.; Gooley, Rebecca M.; Fox, S.; Huxtable, Stewart J.; Belov, Katherine; Pemberton, David; Hogg, Carolyn J.; Grueber, Catherine E. (2018)
      Conservation management relies on baseline demographic data of natural populations. For Tasmanian devils (Sarcophilus harrisii), threatened in the wild by two fatal and transmissible cancers (devil facial tumour disease DFTD: DFT1 and DFT2), understanding the characteristics of healthy populations is crucial for developing adaptive management strategies to bolster populations in the wild....
    • Assessing possible hybridization among managed Nubian ibex in North America

      Putnam, Andrea S.; Nguyen, Tram N.; Mott, Alison; Korody, Marisa L.; Ryder, Oliver A. (2020)
      Hybridization among closely related species is a concern in zoo and aquarium populations where unpedigreed animals are frequently exchanged with the private sector. In this study, we examine possible hybridization in a group of Nubian ibex (Capra nubiana) imported into the Association of Zoos and Aquariums’ (AZA) Species Survival Program (SSP) from a private institution....
    • Benefits of overwintering in the conservation breeding and translocation of a critically endangered amphibian

      Calatayud, Natalie E.; Hammond, Talisin T.; Gardner, Nicole R.; Curtis, Michelle J.; Swaisgood, Ronald R.; Shier, Debra M. (2020)
      At high altitudes, amphibians brumate (over winter) during the winter months, an adaptation that provides protection from harsh weather and minimizes metabolic demand when food resources are scarce. However, brumation in ex situ populations is often avoided due to concerns regarding slow growth rates, compromised immunity, and increased morbidity, and to accelerate growth and sexual maturation. Running counter to these ideas is the hypothesis that husbandry that mimics the environmental conditions under which a species evolved may benefit animal health and reproduction. This may be particularly critical for animals slated for release into the wild. Here, we evaluated the effects of brumation on juvenile southern mountain yellow-legged frogs (Rana muscosa) in a conservation breeding and release program. Growth measurements, (weight and snout-urostyle length [SUL]), were examined in three experimental groups: Nonbrumated, 1 or 3-month brumation. Postrelease survival was also analyzed and compared between nonbrumated and 3-month brumated frogs. This study indicates that brumated R. muscosa juveniles grow to sizes and weights similar to controls within 3 to 4 months following brumation. Mark-recapture models suggested that short-term postrelease survival was not lower and in fact, may be higher in brumated compared to nonbrumated frogs. Results of this study indicate that although brumation entails short-term costs to growth, this species possesses compensatory growth mechanisms following brumation which allow them to attain similar body size to nonbrumated conspecifics in time for the next winter and that for frogs destined for translocation to the wild, brumation could improve survival outcomes.
    • Clinical trials with itraconazole as a treatment for chytrid fungal infections in amphibians

      Brannelly, L.A.; Richards-Zawacki, C.L.; Pessier, Allan P. (2012)
      Due in large part to recent global declines and extinctions, amphibians are the most threatened vertebrate group. Captive assurance colonies may be the only lifeline for some rapidly disappearing species. Maintaining these colonies free of disease represents a challenge to effective amphibian conservation. The fungal disease chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), is one of the major contributors to global amphibian declines and also poses a serious threat to captive assurance colonies. Many treatment options for Bd infection have not been experimentally tested and the commonly administered dosages of some drugs are known to have negative side effects, highlighting a need for clinical trials. The objective of this study was to clinically test the drug itraconazole as a method for curing Bd infection. We bathed Bd-positive juveniles of 2 anuran amphibian species, Litoria caerulea and Incilius nebulifer, in aqueous itraconazole, varying the concentration and duration of treatment, to find the combination that caused the fewest side effects while also reliably ridding animals of Bd. Our results suggest that a bath in 0.0025% itraconazole for 5 min d?1 for 6 d reliably cures Bd infection and causes fewer side effects than the longer treatment times and higher concentrations of this drug that are commonly administered.
    • Deciphering genetic mate choice: Not so simple in group-housed conservation breeding programs

      Farquharson, Katherine A.; Hogg, Carolyn J.; Belov, Katherine; Grueber, Catherine E. (2020)
      Incorporating mate choice into conservation breeding programs can improve reproduction and the retention of natural behaviors. However, different types of genetic-based mate choice can have varied consequences for genetic diversity management. As a result, it is important to examine mechanisms of mate choice in captivity to assess its costs and benefits. Most research in this area has focused on experimental pairing trials; however, this resource-intensive approach is not always feasible in captive settings and can interfere with other management constraints. We used generalized linear mixed models and permutation approaches to investigate overall breeding success in group-housed Tasmanian devils at three nonmutually exclusive mate choice hypotheses: (a) advantage of heterozygous individuals, (b) advantage of dissimilar mates, and (c) optimum genetic distance, using both 1,948 genome-wide SNPs and 12 MHC-linked microsatellites. The managed devil insurance population is the largest such breeding program in Australia and is known to have high variance in reproductive success. We found that nongenetic factors such as age were the best predictors of breeding success in a competitive breeding scenario, with younger females and older males being more successful. We found no evidence of mate choice under the hypotheses tested. Mate choice varies among species and across environments, so we advocate for more studies in realistic captive management contexts as experimental or wild studies may not apply. Conservation managers must weigh up the need to wait for adequate sample sizes to detect mate choice with the risk that genetic changes may occur during this time in captivity. Our study shows that examining and integrating mate choice into the captive management of species housed in realistic, semi-natural group-based contexts may be more difficult than previously considered.
    • Development of a SNP-based assay for measuring genetic diversity in the Tasmanian devil insurance population

      Wright, Belinda; Morris, Katrina; Grueber, Catherine E.; Willet, Cali E.; Gooley, Rebecca; Hogg, Carolyn J.; O’Meally, Denis; Hamede, Rodrigo; Jones, Menna; Wade, Claire; et al. (2015)
      The Tasmanian devil (Sarcophilus harrisii) has undergone a recent, drastic population decline due to the highly contagious devil facial tumor disease. The tumor is one of only two naturally occurring transmissible cancers and is almost inevitably fatal. In 2006 a disease-free insurance population was established to ensure that the Tasmanian devil is protected from extinction. The insurance program is dependent upon preserving as much wild genetic diversity as possible to maximize the success of subsequent reintroductions to the wild. Accurate genotypic data is vital to the success of the program to ensure that loss of genetic diversity does not occur in captivity. Until recently, microsatellite markers have been used to study devil population genetics, however as genetic diversity is low in the devil and potentially decreasing in the captive population, a more sensitive genotyping assay is required.
    • Developmental stability of foraging behavior: evaluating suitability of captive giant pandas for translocation

      Swaisgood, Ronald R.; Martin-Wintle, Meghan S.; Owen, Megan A.; Zhou X.; Zhang H. (2018)
      The behavioral competence of captive-bred individuals - an important source population for translocation programs - may differ from that of wild-born individuals and these differences may influence post-release survival. Some behaviors will be more robust, or developmentally stable, than others in the face of the environmental novelties of captivity. Here, we investigated developmental stability of foraging behavior by quantifying bamboo feeding behavior in captive-bred and wild-born giant pandas, Ailuropoda melanleuca. As an energy-limited species adapted to a low-nutrition diet, any reductions in feeding efficiency may compromise post-release survival. Using video of 22 captive pandas, we measured several components of the panda's elaborate bamboo feeding behavior repertoire. We found that captive-born and wild-born pandas displayed the same repertoire of feeding behaviors, suggesting developmental stability in these motor patterns, but that they employed them differently with different parts of the bamboo. Captive-born pandas devoted less time and effort to handling and chewing leaves while allocating more effort to the consumption of large culms than did wild?born pandas. Captive-born pandas also handled small culm and stripped small culms to prepare them for consumption less often than did wild?born pandas. All of these behavioral differences indicate that wild-born pandas in captivity behave in a manner more similar to wild pandas, and focus their behavioral effort on more nutritious bamboo. Thus, these aspects of captive-born panda feeding behavior may be compromised, and were not developmentally stable in the captive environment. These behavioral differences are cause for concern and should be the subject of future study to determine whether they forecast compromised fitness in translocations. Evaluating developmental stability and behavioral competence should be a key component of captive-release translocation programs, serving to guide pre-release training and selection of individuals to be released.
    • Disentangling the mechanisms of mate choice in a captive koala population

      Brandies, Parice A.; Grueber, Catherine E.; Ivy, Jamie A.; Hogg, Carolyn J.; Belov, Katherine (2018)
      Successful captive breeding programs are crucial to the long-term survival of many threatened species. However, pair incompatibility (breeding failure) limits sustainability of many captive populations. Understanding whether the drivers of this incompatibility are behavioral, genetic, or a combination of both, is crucial to improving breeding programs. We used 28 years of pairing data from the San Diego Zoo koala colony, plus genetic analyses using both major histocompatibility complex (MHC)-linked and non-MHC-linked microsatellite markers, to show that both genetic and non-genetic factors can influence mating success. Male age was reconfirmed to be a contributing factor to the likelihood of a koala pair copulating. This trend could also be related to a pair’s age difference, which was highly correlated with male age in our dataset. Familiarity was reconfirmed to increase the probability of a successful copulation. Our data provided evidence that females select mates based on MHC and genome-wide similarity. Male heterozygosity at MHC class II loci was associated with both pre- and post-copulatory female choice. Genome-wide similarity, and similarity at the MHC class II DAB locus, were also associated with female choice at the post-copulatory level. Finally, certain MHC-linked alleles were associated with either increased or decreased mating success. We predict that utilizing a variety of behavioral and MHC-dependent mate choice mechanisms improves female fitness through increased reproductive success. This study highlights the complexity of mate choice mechanisms in a species, and the importance of ascertaining mate choice mechanisms to improve the success of captive breeding programs.
    • Efforts to restore the California condor to the wild

      Wallace, Michael P. (2012)
      By the early 1980s new studies using radio telemetry and moult patterns to identify individuals indicated that only 21 California condors (Gymnogyps californianus) existed, with five pairs sporadically breeding. With continuous and poorly understood mortality, the decision was made to capture the remaining animals and in 1987 all 27 birds were placed in the protective custody of the San Diego and Los Angeles zoos, at which time the species was considered Extinct in the Wild....
    • Evaluating the performance of captive breeding techniques for conservation hatcheries: A case study of the delta smelt captive breeding program

      Fisch, Kathleen M.; Ivy, Jamie A.; Burton, Ronald S.; May, Bernie (2013)
      The delta smelt, an endangered fish species endemic to the San Francisco Bay-Delta, California, United States, was recently brought into captivity for species preservation. This study retrospectively evaluates the implementation of a genetic management plan for the captive delta smelt population....
    • Giant pandas attend to androgen-related variation in male bleats

      Charlton, Benjamin D.; Swaisgood, Ronald R.; Zhihe, Zhang; Snyder, Rebecca J. (2012)
      Although androgen-dependant traits are predicted to signal overall male quality, no study has examined the response of a nonhuman animal to variation in a known acoustic cue to male androgen levels (steroid hormones that are key drivers of male sexual behaviour). Here, we use a single-speaker approach to present male and female giant pandas with re-synthesised male bleats representing callers with high and low androgen levels. Our results revealed that male and female giant pandas had significantly greater-looking responses, spent more time pacing, and were faster to respond to playbacks of bleats simulating high androgen males. When we analysed the sexes separately, a slightly different response pattern was revealed: whereas males and females still had significantly greater-looking responses and were faster to respond to bleats simulating high androgen males, only male giant pandas tended to spend more time pacing. These findings suggest that vocal cues to male androgen levels are functionally relevant to male and female giant pandas during the breeding season, and constitute the first demonstration that a nonhuman animal could be using a vocal signal to assess male hormonal state. We go on to discuss the ecological relevance of signalling androgen levels in this species’ sexual communication and the possible application of our results to conservation breeding.