Influence of institutional attributes on fulfillment of transfer and breeding recommendations in zoos and aquariums.

Compliance with Breeding and Transfer Plan (BTP) recommendations is important to promote long-term viability and meet the management goals of the Association of Zoos and Aquarium Species Survival Plans (SSPs®). However, individual institutions may fulfill recommendations at different rates, potentially compromising management efforts. We examined institution-level fulfillment rates of BTP recommendations (i.e, "Hold," "Send To," "Breed With," and "Do Not Breed"), and how rates differ based on institutional attributes related to resource levels, geographic location and climate, involvement in population management, and the SSPs in which institutions participated using conditional random forests and generalized linear mixed models. We analyzed 52,182 recommendations from 375 SSPs issued to 170 institutions in BTPs published from 2012 to 2019. Contrary to predictions, our results did not reveal large differences in fulfillment rates based on resources, geographic location, or climate variables at the institution level. We found modest patterns indicating that recommendation fulfillment for Hold and Do Not Breed recommendations in mammals was lower with longer interplanning periods, while fulfillment of Hold recommendations in birds increased with the average experience of individuals in SSP leadership roles. For herptiles, fulfillment of Send To recommendations was moderately higher in institutions with species spread across more herptile taxonomic advisory groups (the management unit for related species). Although our results suggest that overarching institutional factors do not have a strong influence on fulfillment rates at the scale of our study, more focused research within a specific temporal window, taxa, or suite of SSPs may reveal more informative patterns for population management.

Institutional networks in cooperative population management: Exploring patterns in transfer fulfillment.

Long-term sustainability of ex-situ animal populations is important for zoos and aquariums, but challenging due to inconsistent compliance with Breeding and Transfer Plans. Transfer recommendations are key to promoting the sustainability of ex-situ animal populations by ensuring cohesive populations, genetic diversity, and demographic stability, but factors affecting their fulfillment are poorly understood. We used a network analysis framework to analyze data compiled from PMCTrack from 2011 to 2019 for three taxonomic classes (mammals, birds, and reptiles/amphibians) within the Association of Zoos and Aquariums to assess factors affecting transfer recommendation fulfillment. Of 2505 compiled transfer recommendations spanning 330 Species Survival Plan® (SSP) Programs and 156 institutions, 1628 (65%) of them were fulfilled. Transfers were most likely to be fulfilled between institutions in close proximity with an established relationship. Annual operating budget, SSP Coordinator experience, number of staff, and diversity of Taxonomic Advisory Groups in which an institution participates also influenced transfer recommendations and/or fulfillment, but effects varied with taxonomic class. Our results suggest that current practices of focusing on transfers between institutions in close proximity are working to maximize transfer success and that institutions with larger budgets and some degree of taxonomic specialization play important roles in promoting success. Success could be further enhanced by building reciprocal transfer relationships and encouraging further development of relationships between smaller institutions and larger ones. These results emphasize the utility of examining animal transfers using a network approach, which accounts for attributes of both sending and receiving institutions, describing novel patterns otherwise left undetected.

Reasons for unfulfilled breeding and transfer recommendations in zoos and aquariums.

One of the primary tools for cooperatively managing animal populations within the Association of Zoos and Aquariums is through Breeding and Transfer Plan (BTP) recommendations. These recommendations consider population demographics, genetics, husbandry, and institutional needs and aim to improve population viability and long-term sustainability. However, fulfilling (i.e., completing) recommendations can be complicated by biological and logistical challenges. We examined institutional reasons for unfulfilled Breed With, Do Not Breed, Hold, and Send To recommendations collected in surveys in PMCTrack, software for tracking recommendation fulfillment, using descriptive and text-mining methods. Overall, 73 Animal Programs used PMCTrack to distribute 2335 surveys and accrued responses from 167 zoos and aquariums from 2007 to 2019, with a response rate of 56% (n = 1307). For Breed With recommendations, common reasons were related to an individual animal's status and a pair's breeding behavior; for all other recommendation types, reasons were often management or logistical factors. Most Breed With recommendations were attempted (≥55%) but did not result in detectable pregnancy/eggs or offspring, due to pair incompatibility or not enough time to successfully produce offspring. Hold and Do Not Breed recommendations were often unfulfilled because the BTP recommendation was replaced with an interim (i.e., updated) recommendation during the inter-planning period. Our results support the importance of some common population management practices, such as maintaining breeding pairs/groups for multiple BTPs to improve mate familiarity, examining husbandry mechanisms to promote breeding success, and making a concerted effort to adhere to planning timelines to facilitate transfers in alignment with breeding seasons.

Advancing the science behind animal program sustainability: An overview of the special issue.

Over the last ten years, zoos and aquariums around the world have been coming to grips with the "sustainability crisis" - the realization that most of our collaboratively managed animal populations are not viable for the long-term. Many initiatives have been launched at the regional, zoological association, program, and institutional levels to improve the long-term trajectories of these populations. This Special Issue of Zoo Biology highlights some of the scientific approaches that are aimed at addressing population viability and sustainability challenges. The approaches range from development of new analytical tools, to analysis of large datasets, and re-examination of population management principles and philosophies. While much progress has been made in the last ten years, it is clear that continued work on population viability and sustainability is critical and difficult management decisions must be made. In this paper, we identify some of the actions that the zoological community can take to fortify our animal programs and prevent the outright extinction of species.

Uncovering challenges to sustainability of AZA Animal Programs by evaluating the outcomes of breeding and transfer recommendations with PMCTrack.

The Association of Zoos and Aquariums (AZA) cooperatively manages Species Survival Plans® to create demographically and genetically viable populations. SSPs issue animal-specific recommendations to participating institutions via Breeding and Transfer Plans (BTPs). Fulfillment of recommendations is a crucial step in maintaining viable populations, but there have been no comprehensive evaluations of the system. Using PMCTrack, a database of over 110,000 breeding and transfer recommendations issued from over 200 SSPs from 1999 to 2013, we analyzed fulfillment of recommendations. Action-based recommendations had lower rates: Breed With recommendations were fulfilled at a rate of 20.0% before the next BTP, Send To at 56.8%, Do Not Breed at 95.7%, and Hold at 92.9%. We used generalized (logistic) mixed-effects model regressions to evaluate the impact of biological, management, and programmatic factors on fulfillment rates. For all recommendation types, there was significant variation in fulfillment among Programs and within Programs among BTPs. Out of 80 potential hypothesized fixed effects (20 factors * 4 recommendation types), only 20 effects (25%) were statistically significant. Rates were strongly influenced by temporal variables, generally increasing over time and as programs get older. Notably, the amount of time between BTPs was the only variable that significantly predicted fulfillment of all recommendation types. Many additional factors at the individual animal and institutional level may effect fulfillment rates and should be the subject of future analysis. Our results illustrate the utility of PMCTrack and indicate that improvements to the viability of SSPs will need to address multiple biological and management challenges.

PLASMA ELECTROPHORETIC PROFILES IN THE EASTERN MASSASAUGA (SISTRURUS CATENATUS) AND INFLUENCES OF AGE, SEX, YEAR, LOCATION, AND SNAKE FUNGAL DISEASE.

The purpose of this study was to establish reference intervals of the protein electrophoretic fractions and the acute-phase proteins hemoglobin binding protein (as determined by the haptoglobin assay) and C-reactive protein (CRP) and assess any possible correlations between varying age class, sex, location (Illinois or Michigan), year, or presence of snake fungal disease (SFD). Banked plasma samples were assayed from 130 eastern massasaugas from 2009 to 2014 in Illinois and Michigan. Snakes from Michigan had higher total protein (mean: 5.50 g/dl), albumin/globulin ratio (0.42), albumin (1.59 g/dl), and gamma globulins (0.55 g/dl) than from snakes in Illinois (4.72 g/dl, 0.29, 1.03 g/dl, 0.38 g/dl, respectively). Snakes in Illinois (22.19 g/ml) had higher CRP than snakes in Michigan (10.89 mg/ml). Adults had higher gamma globulins (0.47 g/dl) than juveniles (0.28 g/dl). Males had higher alpha-2 globulins (0.98 g/dl) and CRP (21.4 mg/ml) than females (0.85, 11.6, respectively). There were no significant differences in absolute plasma proteins in SFD-positive snakes, but the percentage of gamma globulins was significantly higher in positive snakes. Future research in this area can now build on this data to determine changes in population health over time or due to specific environmental or disease threats.

Extinction risk assessment for the species survival plan (SSP) population of the Bali mynah (Leucopsar rothschildi).

The Bali mynah Species Survival Plan (SSP), an Association of Zoos and Aquariums program, strives to maintain the genetic and demographic health of its population, avoid unplanned changes in size, and minimize the risk of population extinction. The SSP population meets current demographic and genetic objectives with a population size of 209 birds at 61 institutions and 96% genetic diversity (GD) retained from the source population. However, participating institutions have expressed concerns regarding space allocation, target population size (TPS), breeding restrictions, inbreeding depression, and harvest in relation to future population availability and viability. Based on these factors, we assess five questions with a quantitative risk assessment, specifically a population viability analysis (PVA) using ZooRisk software. Using an individual-based stochastic model, we project potential population changes under different conditions (e.g. changes in TPS and genetic management) to identify the most effective management actions. Our projections indicate that under current management conditions, population decline and extinction are unlikely and that although GD will decline over 100 years the projected loss does not exceed levels acceptable to population managers (less than 90% GD retained). Model simulations indicate that the combination of two genetic management strategies (i.e. priority breeding based on mean kinship and inbreeding avoidance) benefits the retention of GD and reduces the accumulation of inbreeding. The current TPS (250) is greater than necessary to minimize the risk of extinction for the SSP population but any reduction in TPS must be accompanied by continued application of genetic management. If carefully planned, birds can be harvested for transfer to Bali for a reintroduction program without jeopardizing the SSP population.

Sex-specific median life expectancies from ex situ populations for 330 animal species.

We present life expectancy estimates for hundreds of vertebrate species based on carefully vetted studbook data from North American zoos and aquariums. These data include sex-specific median life expectancies as well as sample size and 95% confidence limits for each estimate. Existing longevity data for animals primarily consist of maximum lifespan values, which are single observations rather than statistically derived estimates of longevity. Moreover, all of our estimates are based on the same type of data and calculated using consistent, standardized methods. To derive these estimates, we conducted Kaplan-Meier survival analyses using individual-level demographic data (i.e., records of birth and mortality events) from studbook records for each ex situ population. Our species set represents a range of vertebrate taxa (primarily mammals, birds, amphibians, and reptiles) and diverse life histories. This dataset will have broad utility, not only for informing comparative demographic and life history studies, but also more broadly for any research or conservation application that requires sex- or species-specific life expectancy information.

Evaluating the Contribution of North American Zoos and Aquariums to Endangered Species Recovery.

The challenge of recovering threatened species necessitates collaboration among diverse conservation partners. Zoos and aquariums have long partnered with other conservation organizations and government agencies to help recover species through a range of in situ and ex situ conservation projects. These efforts tend to be conducted by individual facilities and for individual species, and thus the scope and magnitude of these actions at the national level are not well understood. Here we evaluate the means and extent to which North American zoos and aquariums contribute to the recovery of species listed under the U.S. Endangered Species Act (ESA), by synthesizing data from federal recovery plans for listed species and from annual surveys conducted by the Association of Zoos and Aquariums. We found that in addition to managing ex situ assurance populations, zoos frequently conduct conservation research and field-based population monitoring and assessments. Cooperatively managed populations in zoos tend to focus on species that are not listed on the ESA or on foreign listings, and thus it may be beneficial for zoos to manage more native threatened species. Our results highlight the existing contributions, but also identify additional opportunities for the zoo community to help recover threatened species.

Climatic and geographic predictors of life history variation in Eastern Massasauga (Sistrurus catenatus): A range-wide synthesis.

Elucidating how life history traits vary geographically is important to understanding variation in population dynamics. Because many aspects of ectotherm life history are climate-dependent, geographic variation in climate is expected to have a large impact on population dynamics through effects on annual survival, body size, growth rate, age at first reproduction, size-fecundity relationship, and reproductive frequency. The Eastern Massasauga (Sistrurus catenatus) is a small, imperiled North American rattlesnake with a distribution centered on the Great Lakes region, where lake effects strongly influence local conditions. To address Eastern Massasauga life history data gaps, we compiled data from 47 study sites representing 38 counties across the range. We used multimodel inference and general linear models with geographic coordinates and annual climate normals as explanatory variables to clarify patterns of variation in life history traits. We found strong evidence for geographic variation in six of nine life history variables. Adult female snout-vent length and neonate mass increased with increasing mean annual precipitation. Litter size decreased with increasing mean temperature, and the size-fecundity relationship and growth prior to first hibernation both increased with increasing latitude. The proportion of gravid females also increased with increasing latitude, but this relationship may be the result of geographically varying detection bias. Our results provide insights into ectotherm life history variation and fill critical data gaps, which will inform Eastern Massasauga conservation efforts by improving biological realism for models of population viability and climate change.

Ecology and Demography of Free-Roaming Domestic Dogs in Rural Villages near Serengeti National Park in Tanzania.

Free-roaming dogs (Canis lupus familiaris) are of public health and conservation concern because of their potential to transmit diseases, such as rabies, to both people and wildlife. Understanding domestic dog population dynamics and how they could potentially be impacted by interventions, such as rabies vaccination, is vital for such disease control efforts. For four years, we measured demographic data on 2,649 free-roaming domestic dogs in four rural villages in Tanzania: two villages with and two without a rabies vaccination campaign. We examined the effects of body condition, sex, age and village on survivorship and reproduction. Furthermore, we compared sources of mortality among villages. We found that adult dogs (>12mos) had higher survival than puppies in all villages. We observed a male-biased sex ratio across all age classes. Overall survival in one non-vaccination village was lower than in the other three villages, all of which had similar survival probabilities. In all villages, dogs in poor body condition had lower survival than dogs in ideal body condition. Sickness and spotted hyena (Crocuta crocuta) predation were the two main causes of dog death. Within vaccination villages, vaccinated dogs had higher survivorship than unvaccinated dogs. Dog population growth, however, was similar in all the villages suggesting village characteristics and ownership practices likely have a greater impact on overall dog population dynamics than vaccination. Free-roaming domestic dogs in rural communities exist in the context of their human owners as well as the surrounding wildlife. Our results did not reveal a clear effect of vaccination programs on domestic dog population dynamics. An investigation of the role of dogs and their care within these communities could provide additional insight for planning and implementing rabies control measures such as mass dog vaccination.