Serving science and conservation: The biological materials request protocol of the New York Zoological Society

Biological materials obtained during routine veterinary treatment and necropsies on zoo and aquarium animals provide opportunities to study a wide variety of phenomena, many of which have important implications for wildlife conservation and captive animal management. Collection and shipment of biological materials require extensive coordination, and few zoological institutions have developed detailed, standardized protocols to facilitate these efforts. The value of using biological materials is reviewed and a set of policies and guidelines are outlined for their collection, preservation, and shipment. Several related issues are discussed, including health hazards and liability issues, permit requirements, and animal welfare considerations.     

Variations in Eastern bongo (Tragelaphus eurycerus isaaci) feeding practices in UK zoological collections

The feeding strategy of the Eastern bongo in the wild is unusual, poorly understood, and few captive feeding recommendations are currently available to zoos. To assess the current state of nutritional husbandry of this rare antelope, eight UK zoos were surveyed. A nutritional husbandry questionnaire was completed and bongos at each zoo were visually assessed by body condition scoring (BCS). Representative samples of the forage and browse consumed by bongos at each zoo were analyzed for nutrient composition using standard agricultural techniques. Significant differences in bongo body condition were found, indicating that zoo husbandry practices are sufficiently varied to have identifiable impacts on the physical condition of the animals. The results highlight a disparity in feeding regimes and diet quality, with significant differences found in forage and browse nutrient compositions and in vitro digestibility. Most forage samples were of a low nutritional quality. Browse provision was found to be largely opportunistic and limited in most zoos. The provision of energy-rich produce was also found to be unnecessary in maintaining a bongo herd at an ideal mean BCS. This survey provides baseline data which may be useful in establishing "good practice" standards for Eastern bongo captive nutrition and highlights several areas requiring further research.     

A Retrospective Study of Mortality in Varanid Lizards (Reptilia:Squamata:Varanidae) at the Bronx Zoo: Implications for Husbandry and Reproductive Management in Zoos

Varanid lizards have been maintained in zoological parks for more than a century, yet few studies to date have attempted to pinpoint significant health issues affecting their management or areas of captive husbandry that are in need of improvement. In an effort to identify and better understand some of the husbandry‐related challenges and health issues specifically affecting varanids in zoos, this study examined mortality in 16 species maintained at the Bronx Zoo between 1968 and 2009. Out of 108 records reviewed, complete necropsy reports were available for 85 individuals. Infection‐related processes including bacterial (15.3%), protozoal (12.9%), nematode (9.4%), and fungal (3.5%) infections accounted for the greatest number of deaths (47.1%). Noninfectious diseases including female reproductive disorders (7.1%), neoplasia (7.1%), gout (10.8%), and hemipenal prolapse (1.3%) accounted for 29.4% of deaths. Multiple disease agents were responsible for 5.9% of deaths, and a cause for death could not be determined for 17.7% of individuals. Reproductive complications accounted for 11.5% of female deaths, but were identified in 23.1% of females. Although not necessarily the cause for death, gout was present in 18.8% of individuals. Differences in mortality between species, genders, and origin (captive‐bred vs. wild‐caught) were also evaluated. The results of this study corroborate earlier findings that identify bacterial infections, neoplasia, female reproductive disorders, gout, and endoparasitism as major sources of mortality in captive varanids. In light of these results, we discuss potential etiologies and offer recommendations for improving captive management practices in zoos. Zoo Biol. 32:152–162, 2013. © 2012 Wiley Periodicals, Inc.     

Captive breeding and infant mortality in Asian elephants: A comparison between twenty western zoos and three eastern elephant centers

Poor reproductive success compromises the long-term viability of captive Asian elephant populations. A questionnaire was designed to assess the importance of reproductive behavior and husbandry factors on breeding success. This was circulated to a number of institutions, zoos, and circuses in Asia, Europe, and North America, all of which kept Asian elephants. The aims were to compare Asian elephant breeding success in different institutions, establish possible causes for any differences, and make recommendations for improving the welfare and breeding success of the animals. The results showed that breeding success in most of the zoos was notably lower and the percentages of stillbirths and infant mortality were relatively higher when compared with those of the institutions in Asia. Female elephants in zoos appeared to reach sexual maturity and reproduce earlier than those in the Asian establishments. However, zoo elephants produced fewer young per female. The different facilities and husbandry methods used are described. Recommendations are made for both short- and long-term changes that could be used to modify existing practices to improve the welfare and breeding success of captive Asian elephants. Zoo Biol 17:311–332, 1998. © 1998 Wiley-Liss, Inc.     

Thirty years later: enrichment practices for captive mammals

Environmental enrichment of captive mammals has been steadily evolving over the past thirty years. For this process to continue, it is first necessary to define current enrichment practices and then identify the factors that limit enhancing the quality and quantity of enrichment, as well as the evaluation of its effectiveness. With the objective of obtaining this information, an international multi‐institutional questionnaire survey was conducted with individuals working with zoo‐housed mammals. Results of the survey showed that regardless of how important different types of enrichment were perceived to be, if providing them was particularly time‐consuming, they were not made available to captive mammals as frequently as those requiring less staff time and effort. The groups of mammals provided with enrichment most frequently received it on average fewer than four times per day, resulting in less than two hours per day spent by each animal care staff member on tasks related to enrichment. The time required for staff to complete other husbandry tasks was the factor most limiting the implementation and evaluation of enrichment. The majority of survey respondents agreed that they would provide more enrichment and carry out more evaluation of enrichment if it was manageable to do so. The results of this study support the need for greater quantity, variety, frequency, and evaluation of enrichment provided to captive mammals housed in zoos without impinging on available staff time. Zoo Biol 29:303–316, 2010. © 2009 Wiley‐Liss, Inc.     

Issues of choice and control in the behaviour of a pair of captive polar bears (Ursus maritimus)

Stereotyped behaviour occurs in a wide variety of captive animals including ursids. The provision of animal control over aspects of their environment by providing choices is a critical element for improving welfare. The behaviour of two sibling polar bears at a metropolitan zoo was examined to investigate the effect of providing access to their indoor, off-exhibit holding space. Both bears demonstrated behavioural changes when given the choice to access their indoor dens including decreased stereotyped behaviours and increased social play. These results, although based on just two bears, provide additional support for the assertion that choice and control are closely tied to issues of well-being for captive animals.     

Black rhinoceros (Diceros bicornis) in U.S. zoos: II. behavior,breeding success,and mortality in relation to housing facilities

The captive population of black rhinoceros (Diceros bicornis) is not self‐sustaining. The reasons for suboptimal reproduction and high mortality need to be investigated. This can only be achieved by cross‐institutional analyses of environments, behavior, and performance. In this study, we collected data on 23 zoos with black rhinoceros to compare zoo environments with reproductive success, mortality, and behavior. Institutional variation was characterized by enclosure area, percentage of walls around enclosure perimeter, percentage of public access along enclosure perimeter, climate, noise level, number of years zoo has maintained black rhinoceros, frequency of chlorine use, and number of male and female black rhinoceros at a zoo simultaneously. Birth and death rates for each institution were calculated from studbook records. We found that the breeding success of a zoo since 1973 correlated positively with enclosure area, and zoos with two or more females had a lower reproductive rate than zoos with only one female. Females residing during their pre‐reproductive years at a zoo with another reproductive female gave birth for the first time on average 3 years later than sole females. Mortality since 1973 correlated positively with percentage of public access. In Part I, we developed behavior profiles of 29.31 individual black rhinoceros from keeper ratings. Scores for males on the behavior trait Fear also correlated positively to percentage of public access, and we suggest that this aspect of black rhinoceros exhibits is a stressor for this species, especially the males. We found that different aspects of captive environments are associated with male and female black rhinoceros behavior. Male scores on the behavior trait dominant were higher in smaller enclosures, and female scores for a group of behaviors suggesting agitation (chasing/stereotypy/mouthing) were positively correlated with percentage of walls in their enclosure. These two behavior traits were found in Part I to be negatively correlated with the breeding success of an individual male or female. We re‐surveyed the behavior and husbandry of 29 black rhinoceros pairs in zoos 2 years after the original data were collected. The re‐survey confirmed that compatible black rhinoceros pairs are those with assertive females and submissive males, and that enclosure area and a low percentage of concrete walls around the enclosure are positive predictors of a pair's reproductive success. We conclude that temperament traits of individuals and characteristics of their captive environments both have an impact on a pair's breeding success. Our study demonstrates that cross‐institutional comparisons of zoo facilities, when integrated with behavioral assessments of individual animals, are a valuable tool for investigating potential causes of poor reproduction and well‐being in zoo animals. Zoo Biol 18:35–52, 1999. © 1999 Wiley‐Liss, Inc.     

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.     

The use of classical and operant conditioning in training Aldabra tortoises (Geochelone gigantea), for venipuncture and other,husbandry issues

A variety of nonhuman animals in zoo and research settings have been the subjects of classical and operant conditioning techniques. Much of the published work has focused on mammals, husbandry training, and veterinary issues. However, several zoos are training reptiles and birds for similar procedures, but there has been little of this work published. Using positive reinforcement techniques enabled the training of 2 male and 2 female Aldabra tortoises (Geochelone gigantea) to approach a target, hold steady on target, and stretch and hold for venipuncture. This article discusses training techniques, venipuncture sight, and future training.     

Single large or several small? Population fragmentation in the captive management of endangered species

Captive populations of endangered species are typically maintained effectively as single random-mating populations by translocating individuals between institutions. Genetic, disease, and cost considerations, however, suggest that this may not be the optimal management strategy. Genetic theory predicts that a pooled population derived from several small isolated populations will have greater genetic diversity, less inbreeding, and less genetic adaptation to captivity than a single large population of equivalent total size, provided there are no population extinctions. These predictions were tested using populations of Drosophila with effective size comparisons of 50 vs. 2 × 25; 100 vs. 2 × 50 vs. 4 × 25, and 500 vs. 2 × 250 vs. 4 × 100 + 2 × 50 vs. 8 × 25 + 6 × 50. Populations were maintained at the indicated sizes as separate pedigreed populations for 50 generations. The several small treatments were subsequently pooled and maintained for eight to 10 generations prior to determination of fitness and evolutionary potential. Several small populations (pooled), when compared to single large populations of equivalent total size, were found to have lower average inbreeding coefficients, significantly higher reproductive fitness under competitive conditions, similar fitness under benign captive conditions, higher genetic diversity, and equivalent evolutionary potential. Trends favored the several small (pooled) populations in all comparisons at population sizes of 50 and 100. We recommend that endangered species in captivity be maintained as several small populations, with occasional exchange of genetic material. This has genetic benefits over current management both in captivity and especially for reintroductions, as well as reducing translocation costs and risks of disease transfer. Zoo Biol 17:467–480, 1998. © 1998 Wiley-Liss, Inc.     

The cryptic genetic structure of the North American captive gorilla population

Western lowland gorillas (Gorilla gorilla gorilla) were imported from across their geographical range to North American zoos from the late 1800s through 1974. The majority of these gorillas were imported with little or no information regarding their original provenance and no information on their genetic relatedness. Here, we analyze 32 microsatellite loci in 144 individuals using a Bayesian clustering method to delineate clusters of individuals among a sample of founders of the captive North American zoo gorilla collection. We infer that the majority of North American zoo founders sampled are distributed into two distinct clusters, and that some individuals are of admixed ancestry. This new information regarding the existence of ancestral genetic population structure in the North American zoo population lays the groundwork for enhanced efforts to conserve the evolutionary units of the western lowland gorilla gene pool. Our data also show that the genetic diversity estimates in the founder population were comparable to those in wild gorilla populations (Mondika and Cross River), and that pairwise relatedness among the founders is no different from that expected for a random mating population. However, the relatively high level of relatedness (R = 0.54) we discovered in a pair of known breeding pairs reveals the need for incorporating genetic relatedness estimates in the captive management of western lowland gorillas.     

Influence of zoo visitor presence on the behavior of captive Indian gaur (Bos gaurus gaurus) in a zoological park

Visitors to zoos can be a source of potential disturbance and stress to some captive, nonhuman animals in the wild. To determine the influence of visitor presence on captive bison (Bos gaurus gaurus), the study analyzed the behavior of 4 individuals at the Arignar Anna Zoological Park, India. The study often observed the behavior of the animals on visitor-present days and on days when visitors were absent. In the presence of zoo visitors, the bison showed a higher level of intragroup aggression and moving behavior. In contrast, the bison rested more when no visitors were present. The results revealed that the presence of zoo visitors significantly influenced the behavior of captive bison and thereby may have affected their welfare.     

Potential contribution of cryopreserved germ plasm to the preservation of genetic diversity and conservation of endangered species in captivity.

Demographic and genetic objectives of captive propagation programs for endangered species focus on establishing demographically secure populations that maintain adequate levels of genetic diversity. Long-term storage and utilization of cryopreserved germ plasm could extend the population's generation length and allow higher levels of genetic variation to be maintained in smaller populations. Since fewer breeding animals would be needed, more species would be "rescued" from extinction using the cage facilities currently available at existing institutions. Doubling generation lengths for callitrichid primates through use of cryopreservation could almost triple the number of species that could be rescued in world zoos. Additionally, long-term cryopreservation would allow for a third population, that of the frozen zoo. Three-way exchange of germ from germ plasm banks to captive and wild populations would increase genetic diversity at reduced risk and expense. Advances in reproductive technology and better understanding of the reproductive physiology of these animal populations are necessary to permit routine application of artificial insemination and embryo transfer using frozen-stored germ plasm.     

Differences in winter activity,courtship, and social behavior of two captive family groups of Mexican wolves (Canis lupus baileyi)

The purpose of this study was to determine differences in activity patterns and social behavior of two groups of endangered Mexican wolves maintained at two quite different facilities and to determine some of the variables that should be considered when making specific behavioral comparisons among wolves in this binational captive breeding program. Quantitative measurements of an Activity Index and social behaviors were obtained for three individuals in each pack. Within each age/sex category, activity, aggression, and play were more frequent in the pack at a zoo facility, compared to the pack at a field station facility. Frequency of courtship interactions and scent marking were significantly higher in the field station pack. The packs were similar in the frequency of active submission, but differed significantly in the pattern of this behavior. Given the large number of interacting variables and small number of individuals in this study, we recommend caution in generalizing results to other packs or facilities. Zoo Biol 16:435–443, 1997. © 1997 Wiley-Liss, Inc.     

A comparative study of litter size and sex composition in a large dataset of callitrichine monkeys

In many birds and mammals, the size and sex composition of litters can have important downstream effects for individual offspring. Primates are model organisms for questions of cooperation and conflict, but the factors shaping interactions among same‐age siblings have been less‐studied in primates because most species bear single young. However, callitrichines (marmosets, tamarins, and lion tamarins) frequently bear litters of two or more, thereby providing the opportunity to ask whether variation in the size and sex composition of litters affects development, survival, and reproduction. To investigate these questions, we compiled a large dataset of nine species of callitrichines (n = 27,080 individuals; Callithrix geoffroyi, Callithrix jacchus, Cebuella pygmaea, Saguinus imperator, Saguinus oedipus, Leontopithecus chrysomelas, Leontopithecus chrysopygus, Leontopithecus rosalia, and Callimico goeldii) from zoo and laboratory populations spanning 80 years (1938–2018). Through this comparative approach, we found several lines of evidence that litter size and sex composition may impact fitness. Singletons have higher survivorship than litter‐born peers and they significantly outperform litter‐born individuals on two measures of reproductive performance. Further, for some species, individuals born in a mixed‐sex litter outperform isosexually‐born individuals (i.e., those born in all‐male or all‐female litters), suggesting that same‐sex competition may limit reproductive performance. We also document several interesting demographic trends. All but one species (C. pygmaea) has a male‐biased birth sex ratio with higher survivorship from birth to sexual maturity among females (although this was significant in only two species). Isosexual litters occurred at the expected frequency (with one exception: C. pygmaea), unlike other animals, where isosexual litters are typically overrepresented. Taken together, our results indicate a modest negative effect of same‐age sibling competition on reproductive output in captive callitrichines. This study also serves to illustrate the value of zoo and laboratory records for biological inquiry.     

Influence of Zoo Visitor Presence on the Behavior of Captive Indian Gaur (Bos gaurus gaurus) in a Zoological Park

Visitors to zoos can be a source of potential disturbance and stress to some captive, nonhuman animals in the wild. To determine the influence of visitor presence on captive bison (Bos gaurus gaurus), the study analyzed the behavior of 4 individuals at the Arignar Anna Zoological Park, India. The study often observed the behavior of the animals on visitor-present days and on days when visitors were absent. In the presence of zoo visitors, the bison showed a higher level of intragroup aggression and moving behavior. In contrast, the bison rested more when no visitors were present. The results revealed that the presence of zoo visitors significantly influenced the behavior of captive bison and thereby may have affected their welfare.     

Can proboscis monkeys be successfully maintained in captivity? A case of swings and roundabouts

Although most western zoos have experienced difficulties in maintaining proboscis monkeys, the Singapore Zoo has managed to sustain a social group of proboscis monkeys housed in a large naturalistic exhibit since 1998. Within 3 years after the monkeys were brought to the zoo, five offspring were produced, all of which survived. Natural forest vegetation from 20 plant species was provided along with a staple diet of about seven different species on a daily basis. The calcium and sodium contents of the plant items consumed by monkeys in the Singapore Zoo were similar to those in the diet of wild proboscis monkeys in Borneo. However, the levels of other minerals, such as iron, magnesium, manganese, potassium, zinc, and phosphorus, were significantly lower in the natural vegetation consumed by the monkeys compared to the wild diet. Food supplements such as primate biscuits, cod liver oil, boiled egg, multivitamins, and mineral syrup further ensured a more balanced diet for the captive monkeys. The data presented here show that zoos can maintain these rare Colobine monkeys successfully by provide them with a natural diet, along with appropriate husbandry and hygiene practices, minimal human interference, and applied nutritional science. The husbandry and nutritional management model presented in this paper could be of use to other institutions around the world. Zoo Biol 23:533–544, 2004. © 2004 Wiley-Liss, Inc.     

Husbandry, handling, and nutrition for marmosets

Marmosets, especially Callithrix jacchus, have become an established part of the laboratory animal community. Information on marmoset life history, behavior, and diet acquired from experience with natural and captive habitats has increased, but the early information from workers with colonies, principally those of tamarins, has led to some common perceptions about how to house, handle, and especially, feed callitrichids that may not apply to marmoset requirements. The availability of commercially produced, almost-complete base diet components and a wider variety of cage construction materials, combined with the recent emphasis on the integration of engineering and performance standards for housing, have made captive life and the implementation of research requirements better for the animals and the people that work with them. We will review some of the routine aspects of husbandry, handling, and nutrition for marmoset monkeys maintained in a research setting.     

The Welfare of Bears in Zoos: A Case Study of Poland

The welfare of captive bears became a big issue of concern in Poland when a case of a bear being ill-treated became a high-profile case in the media. This case created a challenge to verify, study, and understand the main problems associated with bear keeping so that zoos could significantly improve the conditions in which they keep bears or ensure they keep bears at the minimum required standards. The results presented here are from 1 of the few countrywide studies of captive bear conditions conducted in all the captive institutions in Poland that keep bears. Thirteen institutions kept bears at the time of the study (2007–2009), including 54 individuals of 5 species. Major welfare problems were identified, and the results have been used to challenge zoos to address the changes required and focus the government's attention on areas that require legislative improvement.     

Public Attitudes in India and Australia toward Elephants in Zoos

ABSTRACT

We surveyed the attitudes of people toward captive elephants in australia, where importation into zoos has been controversial recently, compared with India, where elephants are indigenous. Both australian (AR, n = 101) and Indian (IR, n = 101) respondents rated conservation as the most important reason for the role of zoos and sanctuaries. Australian respondents were more concerned about the husbandry conditions for keeping wild animals in zoos and sanctuaries than Indian respondents (p = 0.02). This concern for captive animals increased with the higher educational level of the respondents. Female australian respondents were more concerned about the practice of keeping elephants in captivity than australian men. More australian respondents were prepared to pay extra to visit a zoo with elephants (AR 42.6%, IR 7.9%, p < 0.001). Indian respondents believed more than their australian counterparts that it was important for any zoo to display elephants, and wanted to interact with elephants by feeding, touching, and riding on them. While australian respondents? perceptions of captive elephants acknowledged their scientific value, Indian respondents viewed elephants primarily of religious, cultural, and historical significance. We conclude that australians and Indians have different requirements for keeping elephants in zoos, which should inform zoo directors about the best way to present them to the public.