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.     

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.     

Survey and interzoo studies used to address husbandry problems in some zoo vertebrates

In addition to genetic and demographic considerations, SSP coordinators have been asked to systematically address husbandry issues. Three approaches to the study of captive management issues are typically used: (1) large numbers of individuals are housed at a single institution maintained in a situation that facilitates systematic evaluation of the captive environment, (2) an investigator travels to many institutions to gather data on a single taxon, or (3) an investigator surveys existing information by assembling data from a large number of individuals at a variety of institutions. Each approach has both advantages and disadvantages in terms of feasibility and the type of results obtained. The use of surveys to obtain information about husbandry parameters from a large number of animals maintained at a variety of zoos is quite possibly the most common approach used among zoo managers. Zoo husbandry surveys are typically developed to address issues problematic to a particular species, including reproductive failure and health issues. Unfortunately, surveys appear to be an often misused research tool among zoo professionals. Surveys can be improved by working with psychologists or sociologists at local universities, by narrowing the focus of the survey's purpose, and by carefully constructing each question. © 1994 Wiley-Liss, Inc.     

History and dietary husbandry of pangolins in captivity

The objective of this study was to establish a history of feeding and dietary husbandry of pangolin in captivity. Over the past 150 years, several zoos have attempted to maintain pangolins (Manis spp). Most of these zoos have not succeeded in maintaining these animals for long periods, associated largely with dietary problems. This study reviews the historic records of captive pangolins. The dietary husbandry of pangolins in Taipei Zoo is discussed in detail. Zoo Biol 0:1–8, 2007. © 2007 Wiley‐Liss, Inc.     

Causes of mortality in captive cotton‐top tamarins (Saguinus oedipus)

Cotton‐top tamarins have been housed in captivity in the United States for over five decades. These animals initially were managed in biomedical and research facilities, and more recently have been kept in zoos as well. Although the causes of mortality in captive cotton‐top tamarins have been a topic of investigation for biomedical colonies, they have not been addressed for the North American zoo population. In this retrospective study we review the causes of mortality in the AZA Cotton‐top Tamarin Species Survival Plan (SSP)© population during 1997–2001 to assess current husbandry practices and assist in further developing effective husbandry and management programs for this endangered species. Zoo Biol 23:127–137, 2004. © 2004 Wiley‐Liss, Inc.     

Life span,reproductive output,and reproductive opportunity in captive Goeldi's monkeys (Callimico goeldii)

In the absence of long‐term field studies, demographic and reproductive records from animals housed in zoos and research laboratories are a valuable tool for the study of life history variables relating to reproduction. In this study, we analyzed studbook records of more than 2,000 individuals born over a 40‐year period (1965–2004) to describe life history patterns of captive Goeldi's monkeys (Callimico goeldii) housed in North America and Europe. Using Kaplan–Meier survival analysis methods, we found the mean life span to be 5.5 years. The rate of infant mortality, defined as death before 30 days, was approximately 30%, with European animals being more likely to survive infancy than North American animals. When individuals surviving at least 1.5 years are considered, lifetime reproductive output averaged 3.5 offspring, yet more than one‐third of individuals did not produce any offspring. Using a smaller dataset of individuals with known pairing histories, we developed a measure of opportunity for reproduction (OFR), which represented the total time an individual was known to be housed with a potential mate. For both sexes, we found that the correlation between OFR and number of offspring produced was much higher than the correlation between life span and number of offspring produced. This result highlights the importance of taking into account an individual's OFR. As a whole, our findings help characterize the life histories of captive Goeldi's monkeys and emphasize the impact management practices may have on reproductive success. Zoo Biol 29:1–15, 2010. © 2009 Wiley‐Liss, Inc.     

Familiarity During Immaturity: Implications for the Captive Propagation of Gibbons

Immature captive gibbons are often housed together to facilitate healthy social development. Zoo personnel have wondered if the familiarity acquired during peer-rearing results in sexual aversion at maturity. We discuss whether housing gibbons together before sexual maturity causes them to later reject each other as mates and therefore inhibits their reproductive potential. We conducted a survey of gibbons housed at zoos, conservation centers, and with private individuals. Our data suggest that early rearing experiences with potential mates do not prevent mating between gibbons housed together while immature. Using studbook data, we compared infant mortality in inbred and outbred captive gibbons. We found no significant difference in mortality rates for the 2 samples, though adverse effects of inbreeding may become apparent at later ages and in future generations. Our results indicate that early cohabitation is a feasible housing strategy for breeding programs and for rehabilitation/rescue projects in habitat countries where the main concern is the reproductive viability of gibbons.     

Optimal conditions for breeding of captive humboldt penguins (Spheniscus humboldti): A survey of British zoos

We surveyed 16 British zoos and bird gardens to assess the optimal conditions for breeding of captive Humboldt penguins (Spheniscus humboldti). We obtained information on population, enclosure, and husbandry characteristics and related these variables to three measures of per capita breeding success, namely, per capita egg productivity, chick productivity, and hatching success (measured as the proportion of eggs laid that hatched). All three fitness measures increased with an increasing number of breeding pairs and total population size but were not related to population density. Once the effect of number of breeding pairs was removed statistically, chick productivity was found to be highest when nesting boxes were lined with sand and gravel instead of alternative substrata such as twigs or vegetation. Hatching success increased with increasing pool size and was highest in enclosures with concrete floors. Adult mortality in zoos was generally low and appeared related to the use of chlorine in freshwater pools and to the presence of other penguin species in Humboldt penguin displays. Several enclosure and husbandry parameters were not variable enough to assess their impact on reproduction of captive Humboldt penguins. Recommendations for optimising conditions for captive breeding of Humboldt penguins include keeping as large a population as possible in a concrete enclosure with a large pool area, while providing sand and gravel as nesting material. Bird density may be important but we did not detect detrimental effects on breeding for densities up to 0.25 birds m^–2. Adult mortality can be minimised by exhibiting Humboldt penguins in single‐species display and avoiding chlorination of pool water. An experimental approach is recommended to confirm the results of this correlational study. Zoo Biol 20:545–555, 2001. © 2002 Wiley‐Liss, Inc.     

Retrospective study of morbidity and mortality of captive jaguars (Panthera onca) in North America: 1982–2002

One hundred seventy‐two medical records of captive jaguars (Panthera onca) were examined from 30 American Zoo and Aquarium Association (AZA) institutions housing jaguars between 1982–2002. The study determined common causes of morbidity and mortality, and the influence of age, gender, and melengestrol‐acetate (MGA) exposure on these rates. The most common causes of morbidity in captive jaguars were found to be dental, gastrointestinal, integumentary, and musculoskeletal diseases. Prevalence of types of disease varied with age, with older animals experiencing a higher prevalence of multiple types of disease. Females developed reproductive disease more frequently than males, and the data suggest that MGA exposure increased the risk of developing female reproductive disease. The most common causes of mortality were reproductive diseases in females and musculoskeletal diseases in males. There was a high rate of neonate and pediatric mortality, primarily due to stillbirths or unexplained neonatal death, trauma, and pneumonia. Other diseases or clinical signs that seemed remarkable were a high prevalence of episodes of epistaxis among young, as well as old, jaguars. Based on these findings, management suggestions for the captive jaguar population are presented. Zoo Biol 0:1–12, 2006. © 2006 Wiley‐Liss, Inc.     

Birth sex ratio in captive mammals: Patterns,biases, and the implications for management and conservation

Sex allocation theory predicts that a female should produce the offspring of the sex that most increases her own fitness. For polygynous species, this means that females in superior condition should bias offspring production toward the sex with greater variation in lifetime reproductive success, which is typically males. Captive mammal populations are generally kept in good nutritional condition with low levels of stress, and thus populations of polygynous species might be expected to have birth sex ratios biased toward males. Sex allocation theory also predicts that when competition reduces reproductive success of the mother, she should bias offspring toward whichever sex disperses. These predicted biases would have a large impact on captive breeding programs because unbalanced sex ratios may compromise use of limited space in zoos. We examined 66 species of mammals from three taxonomic orders (primates, ungulates, and carnivores) maintained in North American zoos for evidence of birth sex ratio bias. Contrary to our expectations, we found no evidence of bias toward male births in polygynous populations. We did find evidence that birth sex ratios of primates are male biased and that, within primates, offspring sex was biased toward the naturally dispersing sex. We also found that most species experienced long contiguous periods of at least 7 years with either male‐ or female‐biased sex ratios, owing in part to patterns of dispersal (for primates) and/or to stochastic causes. Population managers must be ready to compensate for significant biases in birth sex ratio based on dispersal and stochasticity. Zoo Biol 19:11–25, 2000. © 2000 Wiley‐Liss, Inc.     

Breeding orangutans at Perth Zoo: Twenty years of appropriate husbandry

The Perth Zoo orang-utan husbandry strategy, which has been the foundation of 20 years of success in breeding, health, and longevity, is based on respect for the solitary arboreal nature of the species. The orang-utans are housed singly at night and fed only in their night dens. Diets are based on the weight and energy expenditure of the individuals. During the day they are housed singly or in very small groups that correspond in size and structure to wild population units. Adult males and females are only introduced for breeding purposes. Large climbing frames, which permit visual and vocal contact, dominate the day enclosures. A wide variety of manipulable objects are provided daily to enhance activity levels. Since 1968 there have been 21 births, 14 surviving infants, and no post-infancy deaths. All the mature animals are fertile. The major health problems of captive orang-utans and the most common causes of adult mortality have been absent from the colony. The husbandry method used has made it possible to record detailed reproductive data including complete menstrual cycle records for 8 females since 1981, the observation and quantification of cyclic proceptivity for all mature females, the calculation of 19 gestation periods, and the measurement of post-partum amenorrhea and interbirth intervals. Urinary hormone analysis is used regularly to confirm ovulation. A long-term study of the hormones mediating the development of secondary sexual characteristics in males was started in 1988. Captive orang-utans do not have a fertility problem, but the captive population is threatened by the unacceptably high mortality rate in young adults. This appears to be related to inappropriate husbandry methods. The most neglected aspect of orang-utan husbandry is natural social group size and structure.     

Elephant importation from range countries: ethical and practical considerations for accredited zoos

Zoo elephant populations are in serious demographic peril. Advances in elephant management and care are expected to lead to improved reproductive success. The existing cohort of reproductively viable adult females is aging, however, and effective changes may not come fast enough to sustain the population over time. If so, importation of captive, semi‐domesticated, and wild elephants from range countries may be necessary for zoo programs to survive. Yet, due to the high profile elephants now have with animal rights activists, there may be increasing legal and political barriers to elephant importation. This makes it especially important that zoos become more proactive in addressing remaining weaknesses in elephant management and care and building the case for elephants in zoos. This article summarizes the key considerations for AZA‐accredited zoos that are contemplating future importations. These include ethical, legal, practical, public relations, and other considerations. The authors strongly recommend that zoos position themselves for possible future importations immediately instead of waiting until the last minute. It is equally critical that zoos recognize their existing vulnerabilities and attempt to address them proactively; only then, can they take control of their own fate and reduce the potential for later regret. Zoo Biol 25:219–233, 2006. © 2006 Wiley‐Liss, Inc.     

Body weights of ruffed lemurs (Varecia variegata) in European zoos with reference to the problem of obesity

Qualitative observations in several European zoos revealed a high proportion of obese individuals in different species of lemurs. This phenomenon was examined in both subspecies of the ruffed lemur (Varecia variegata variegata and Varecia variegata rubra). Data on body weight were obtained from 43 animals in 13 European zoos and were compared with body weights of wild ruffed lemurs. The captive individuals’ mean weight was significantly higher than either of two different samples of wild V. variegata variegata. Using a weight‐based definition of obesity, 46.5% of the individuals in our sample were obese. Neither significant differences in body weight between the two subspecies nor between sexes could be found. Body weight did not correlate with age. The findings are discussed with reference to the feeding ecology of ruffed lemurs and their nutrition in captivity and to implications for captive breeding programs for this species. Zoo Biol 20:261–269, 2001. © 2001 Wiley‐Liss, Inc.     

A Case Study of Malayan Tapir (Tapirus indicus) Husbandry Practice Across 10 Zoological Collections

The Malayan, or Asian, tapir (Tapirus indicus) has a diminishing wild population and is becoming more common in captivity as zoos attempt to manage sustainable ex situ populations. Tapirs can be relatively easy to maintain and breed, but captive animals appear to suffer from reduced activity budgets, obesity, and poor public image. A questionnaire‐based survey was designed and sent specifically to 10 collections around the world that exhibit Malayan tapirs, with the aim of assessing husbandry regimes to determine prevalence of standardized practices as well as highlighting any key differences, and to showcase good practice, thus providing information beneficial to those maintaining this species in their zoo. Twenty‐five animals were included in the survey from collections across four continents. The research's major conclusions show differing dietary make‐up, with a lack of forage provision, contrasting with a diverse array of enrichment protocols used. Significant differences were noted between zoos for total amount of food offered (P = 0.000) as well as ratios of forage to concentrate pellet offered (P = 0.004). Comparing food offered to male and female tapirs with published requirements for an “average” of either gender shows not all zoos providing the amount suggested in husbandry guidelines. Intelligently designed and original enrichment was provided to all animals but differences between zoos were noted in the application and “usefulness” of enrichment for individual tapir. Overall, animals are benefiting from enrichment but welfare could be further improved via consistent feeding of ad libitum forage and regular use of browse as a constituent part of daily rations. Zoo Biol. 32:347–356, 2013. © 2012 Wiley Periodicals, Inc.     

Sexual behavior and hormonal estrus cycles in captive aged lowland gorillas (Gorilla gorilla)

To evaluate whether observed cycles in proceptive behavior in aging lowland gorilla females (age 40+) at Brookfield Zoo were driven by ovarian activity, we compared monthly behavioral data to estradiol and progestogen cycles based on fecal hormone assessments. Progestogen peaks showed regularity and close coincidence with monthly sexual behaviors. Estradiol was more variable. Progestogen peaks varied between 22+/-5 days for the control female (29 years old), to 24+/-2.5 and 29+/-8 for the two aged subjects. In the first aged female, which was housed with other females and a silverback, the high degree of cyclicity in sexual behavior, regularity of progestogen cycles, and close concordance between hormonal cycling and sexual behavior strongly compared to patterns found (in this and other studies) in gorilla females <35 years old. Cyclical progestogen peaks were longer and more variable in the second aged female-perhaps because she lacked the social mediation of other females or a male. For husbandry reasons she is not housed with the gorilla group, behavioral data were not collected from her. The value of our longitudinal study is in obtaining reproductive profiles of primate females that are approaching maximum lifespan. This pilot study is part of a larger research project on reproductive senescence that will include other captive females >35 years old, a population that is rapidly increasing in North American zoos as gorillas continue to age.     

Welfare evaluations of nonhuman animals in selected zoos in the Philippines

This study evaluated 3 zoos in the Philippines: the Wildlife Rescue Center and Mini Zoo, Manila Zoological and Botanical Garden, and Cavite Botanical and Zoological Park to determine the standards of nonhuman animal welfare. The study measured and compared the cage sizes of various animals to the international minimum standards. According to the categories of management and husbandry, the 3 zoos showed a significant difference on the mean scores of ranking. The Wildlife Rescue Center and Mini Zoo ranked first, followed by Manila Zoo and Cavite Zoo. Although most cages in the 3 zoos followed acceptable minimum standards, the study identified several problems related to animal welfare, hygiene, husbandry, and management. Based on the evaluations, the study recommended that the 3 zoos improve animal welfare standards.     

Environmental influences on stereotypy and the activity budget of Indian leopards (Panthera pardus) in four zoos in Southern India

To eliminate abnormal behaviors in leopards (Panthera pardus), such as stereotypic pacing, by utilizing environmental enrichment techniques, a proper understanding of their behavior in captive environments is required. Hence there is a need for animal welfare studies in Indian zoos. The activity budgets of 16 leopards were recorded across four southern Indian zoos: Thiruvananthapuram Zoo, Arignar Anna Zoological Park, Shri Chamarajendra Zoological Gardens, and the Guindy Children's Park. Of the 16 study animals, 14 were studied on‐exhibit on zoo holidays as well as on days with visitors present, and all 16 individuals were studied off‐exhibit on other days with visitors present. The 11 behaviors recorded were categorized into active, resting, and stereotypic behaviors. Leopards exhibited higher levels of activity in the on‐exhibit enclosures on days with no visitors. Feeding time influenced the behavioral repertoire of all 14 leopards studied on‐exhibit. Lower proportions of resting were exhibited during the hours before feeding. The proportion of active behaviors differed significantly across zoos. Stereotypic pacing levels were not influenced by the presence of visitors or by feeding time, but was significantly influenced by enclosure features. Higher levels of stereotypic pacing were exhibited in off‐exhibit than on‐exhibit enclosures. Our study shows that the behavior of captive leopards is influenced by enclosure type, feeding regime, and the presence of visitors. Zoo Biol 21:585–595, 2002. © 2002 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.     

Preliminary Findings of Fecal Gonadal Hormone Concentrations in Six Captive Sea Otters (Enhydra lutris) after Deslorelin Implantation

The sea otter (Enhydra lutris) is a popular exhibit animal in many zoos and aquariums worldwide. Captive sea otters from these populations are owned by the United States Fish and Wildlife Service (USFWS). The USFWS has requested that these sea otters be prevented from breeding in order to save captive space for wild rescued animals. Sea otters are often housed in mixed sex groups, therefore a chemical contraceptive method or surgical removal of gonads must be used to prevent potential pregnancy. The contraceptive, Suprelorin® or deslorelin, has been used in many different species to effectively suppress reproduction but duration of effect may vary not only between species but also individuals. Here, we report the effects of one to several consecutive deslorelin implants on gonadal reproductive hormones found in fecal samples from six captive sea otters (two males and four females) compared to two control otters (one male and one female) housed at three zoological institutions. We documented the longitudinal hormone signatures of many stages of the contraceptive cycle including pretreatment (PT), stimulatory phase (S), effective contraception (EC), and hormone reversal (HR) that was characterized by a return to normal hormone levels. Deslorelin was found to be an effective contraceptive in sea otters and was found to be reversible documented by a live birth following treatment, however the duration of suppression in females was much longer than expected with a 6‐month and a 1‐year implant lasting between 3 and 4 years in females. Zoo Biol. 32:307–315, 2013. © 2012 Wiley Periodicals, Inc.     

Reproductive parameters and life-history variables in captive golden-bellied mangabeys (Cercocebus agilis chrysogaster)

An understanding of the reproductive physiology of captive primates is vital for their successful management. We report on reproductive parameters and life-history variables collected at the Sacramento Zoo for five female golden-bellied mangabeys (Cercocebus agilis chrysogaster) over a 7-year period. For each female, we collected data on their sexual skins, menses, gestation, and other pregnancy-related factors, such as postconception bleeding and swelling. We used these data to estimate life-history variables, such as age at onset of estrus, menses, and conception, as well as the duration of intervals between births, and between parturition and the resumption of cycling. Cercocebus agilis chrysogaster is comparable to other Cercocebus species in terms of reproductive parameters, although variability is exhibited within and among female subjects. In some cases, it appears that stressful incidents altered cycle length or halted cycling altogether. We suggest the use of husbandry practices that include consistent data collection to enhance regularity in reproductive cycles, and maximize captive breeding success for this rare species.