The Sizes of Elephant Groups in Zoos: Implications for Elephant Welfare

This study examined the distribution of 495 Asian elephants (Elephas maximus) and 336 African elephants (Loxodonta africana) in 194 zoos, most of which were located in Europe (49.1%) and North America (32.6%). Cows outnumbered bulls 4 to 1 (Loxodonta) and 3 to 1 (Elephas). Groups contained 7 or fewer: mean, 4.28 (σ = 5.73). One fifth of elephants lived alone or with one conspecific. Forty-six elephants (5.5%) had no conspecific. Many zoos ignore minimum group sizes of regional zoo association guidelines. The American Zoo and Aquarium Association recommends that breeding facilities keep herds of 6 to 12 elephants. The British and Irish Association of Zoos and Aquariums recommends keeping together at least 4 cows over 2 years old. Over 69% Asian and 80% African cow groups—including those under 2 years—consisted of fewer than 4 individuals. Recently, Europe and North America have made progress with some zoos no longer keeping elephants and with others investing in improved facilities and forming larger herds. The welfare of individual elephants should outweigh all other considerations; zoos should urgently seek to integrate small groups into larger herds.     

Variation in nature: its implications for zoo elephant management

Despite many advances in animal care and welfare over the past few decades, zoos have been criticized recently for the quality of their elephant management programs. More specifically, critics have argued that elephants live miserable lives in captivity and thus should not be kept in zoos. Poor health and reproductive success, they say, are the result of the combined impact of: a lack of exercise; exposure to cold temperatures and disease; and stress due to the use of “brutal” training techniques, chaining and inappropriate social environments. Everyone, including zoo professionals, seems to agree that improvements in zoo elephant management are necessary and appropriate. However, there is considerable disagreement on how to proceed and little information on which to base such decisions. One tactic that the critics have adopted in their efforts to promote change is their frequent reference to “nature” as a yardstick for gauging the adequacy of zoo animal management and care. An argument is made that direct zoo–wild comparisons are of questionable utility and may be invalid from a scientific perspective. Some critics talk about “nature” as if it represented a fixed set of rules by which captive managers must either abide by or risk diminishing the health and welfare of their charges. However, many aspects of elephant natural history vary greatly depending on prevailing environmental conditions and elephants may be much more flexible than many critics are giving them credit for. Thus, although zoo animal managers should look to nature for clues about how to best care for captive elephants, they should not feel constrained by them. This revelation is not intended as an excuse for poor elephant management or to support the status quo. On the contrary, a better approach is to develop realistic and biologically meaningful metrics that reflect the quality of elephant care and welfare and to use them to measure the success of evolving zoo elephant programs. Zoo Biol 25:161–171, 2006. © 2006 Wiley‐Liss, Inc.     

Diurnal variation of salivary cortisol in captive African elephants (Loxodonta africana) under routine management conditions and in relation to a translocation event

The present study assessed the diurnal variation in salivary cortisol in captive African elephants during routine management (baseline) and in relation to a potential stressor (translocation) to evaluate to what extent acute stress may affect diurnal cortisol patterns. Under baseline conditions, we collected morning and afternoon saliva samples of 10 animals (three zoos) on different days in two study periods (n = 3–10 per animal, daytime and period). Under stress conditions, we sampled the transported cow (newcomer) and the two cows of the destination zoo before and after the transport in the morning and afternoon (n = 3–9 per animal, daytime and transport phase), as well as after the first introduction of the newcomer to the bull (n = 1 per animal). Cortisol was measured in unextracted samples by enzyme immunoassay. Under baseline conditions, we observed the expected diurnal variation with higher cortisol levels in the morning than in the afternoon. Under stress conditions, neither a significant difference between pre- and posttransport, nor between morning and afternoon levels was found. The percentage difference between morning and afternoon cortisol after the transport, however, was remarkably lower than before the transport in the newcomer potentially indicating a stress response to familiarization. Saliva samples taken immediately after the introduction of the newcomer to the bull revealed a marked cortisol increase. Our findings indicate that stressors may disturb the diurnal cortisol rhythm. Furthermore, provided that samples can be collected promptly, salivary cortisol is a useful minimally invasive measure of physiological stress in the African elephant.     

Skewed birth sex ratio and premature mortality in elephants

Sex allocation theories predict equal offspring number of both sexes unless differential investment is required or some competition exists. Left undisturbed, elephants reproduce well and in approximately even numbers in the wild. We report an excess of males are born and substantial juvenile mortality occurs, perinatally, in captivity. Studbook data on captive births (CB, n = 487) and premature deaths (PD, <5 years of age; n = 164) in Asian and African elephants in Europe and North America were compared with data on Myanmar timber (Asian) elephants (CB, n = 3070; PD, n = 738). Growth in CB was found in three of the captive populations. A significant excess of male births occurred in European Asian elephants (ratio: 0.61, P = 0.044) and in births following artificial insemination (0.83, P = 0.003), and a numerical inclination in North American African elephants (0.6). While juvenile mortality in European African and Myanmar populations was 21–23%, it was almost double (40–45%) in all other captive populations. In zoo populations, 68–91% of PD were within 1 month of birth with stillbirth and infanticide being major causes. In Myanmar, 62% of juvenile deaths were at >6 months with maternal insufficient milk production, natural hazards and accidents being the main causes. European Asian and Myanmar elephants PD was biased towards males (0.71, P = 0.024 and 0.56, P < 0.001, respectively). The skewed birth sex ratio and high juvenile mortality hinder efforts to help captive populations become self-sustaining. Efforts should be invested to identify the mechanism behind these trends and seek solutions for them.     

Causes and correlates of calf mortality in captive Asian elephants (Elephas maximus)

Juvenile mortality is a key factor influencing population growth rate in density-independent, predation-free, well-managed captive populations. Currently at least a quarter of all Asian elephants live in captivity, but both the wild and captive populations are unsustainable with the present fertility and calf mortality rates. Despite the need for detailed data on calf mortality to manage effectively populations and to minimize the need for capture from the wild, very little is known of the causes and correlates of calf mortality in Asian elephants. Here we use the world''s largest multigenerational demographic dataset on a semi-captive population of Asian elephants compiled from timber camps in Myanmar to investigate the survival of calves (n = 1020) to age five born to captive-born mothers (n = 391) between 1960 and 1999. Mortality risk varied significantly across different ages and was higher for males at any age. Maternal reproductive history was associated with large differences in both stillbirth and liveborn mortality risk: first-time mothers had a higher risk of calf loss as did mothers producing another calf soon (<3.7 years) after a previous birth, and when giving birth at older age. Stillbirth (4%) and pre-weaning mortality (25.6%) were considerably lower than those reported for zoo elephants and used in published population viability analyses. A large proportion of deaths were caused by accidents and lack of maternal milk/calf weakness which both might be partly preventable by supplementary feeding of mothers and calves and work reduction of high-risk mothers. Our results on Myanmar timber elephants with an extensive keeping system provide an important comparison to compromised survivorship reported in zoo elephants. They have implications for improving captive working elephant management systems in range countries and for refining population viability analyses with realistic parameter values in order to predict future population size of the Asian elephant.     

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.     

Research in zoos: a growth area in conservation

Despite early menageries being the source of much useful biological information on anatomy and taxonomy, it is only more recently that the potential for research in zoos has been recongnized. Collections of captive animals are unique and irreplaceable resources for conservation; but without research in zoological parks, progress in conservation science would diminish. There is a flow of information from zoo researchers to field scientists that assists in providing new insights into species biology. Reciprocally, data collected in the field enhance efforts in captive breeding. This paper summarizes the new research initiatives undertaken in zoos, e.g., in the fields of reproductive and genetic technologies, and highlights their significance for conservation and management of threatened species. It is evident that zoo research has a vital role in linking in situ and ex situ conservation. This role needs to be expanded and developed to meet the challenge posed by expanding human and declining wildlife populations and ecosystems.     

Disease risk and inter‐institutional transfer of specimens in cooperative breeding programs: Herpes and the elephant species survival plans

Managers of cooperative breeding programs and re‐introduction projects are increasingly concerned with the risk of disease transmission when specimens are transferred among facilities or between facilities and the natural environment. We used data maintained in North American studbooks to estimate the potential risks of disease transmission by direct and indirect contact of specimens in the American Zoo and Aquarium Association’s Elephant Species Survival Plan. Histological evidence for a novel herpesvirus disease transmitted between and within elephant species housed in North American facilities prompted an examination of the scope of possible transmission routes within the captive population. We found that, compared with other species managed through Species Survival Plans, elephants experience relatively few transfers between zoos. Nevertheless, the number of direct contacts with other elephants born during the study period of 1983–1996 (excluding stillbirths) was much higher than we had anticipated (μ = 25 ± 27; N = 59) and the number of potential indirect contacts was surprisingly large (μ = 143 ± 92; N = 59). Although these high rates of potential contacts complicate exact identification of infection pathways for herpesvirus, we were able to propose potential routes of transmission for the histologically identified cases. Furthermore, the extraction of data from studbooks allowed us to readily identify other specimens that did not succumb to the disease despite similar exposure. Moreover, we were able to identify other possible cases to recommend for histological examination. Herein we reveal the possibilities of multiple disease transmission pathways and demonstrate how complex the patterns of transmission can be, confounded by the unknown latency of this novel herpesvirus. This emphasizes the need for zoo veterinarians and cooperative breeding programs to consider the full potential for disease transmission associated with each and every inter‐zoo transfer of specimens. Zoo Biol 20:89–101, 2001. © 2001 Wiley‐Liss, Inc.     

Blood‐feeding ecology of mosquitoes in zoos

To determine if the unique host assemblages in zoos influence blood‐feeding by mosquitoes (Diptera: Culicidae), a sampling programme was conducted in Greenville and Riverbanks Zoos, South Carolina, U.S.A., from April 2009 to October 2010. A total of 4355 female mosquitoes of 14 species were collected, of which 106 individuals of nine species were blood‐fed. The most common taxa were Aedes albopictus (Skuse), Aedes triseriatus (Say), Anopheles punctipennis (Say), Culex erraticus (Dyar & Knab), Culex pipiens complex (L.) and Culex restuans (Theobald). Molecular analyses (cytochrome b) of bloodmeals revealed that mosquitoes fed on captive animals, humans and wildlife, and took mixed bloodmeals. Host species included one amphibian, 16 birds, 10 mammals (including humans) and two reptiles. Minimum dispersal distances after feeding on captive hosts ranged from 15.5 m to 327.0 m. Mosquito–host associations generally conformed to previous accounts, indicating that mosquito behaviour inside zoos reflects that outside zoos. However, novel variation in host use, including new, exotic host records, warrants further investigation. Zoos, thus, can be used as experiment environments in which to study mosquito behaviour, and the findings extrapolated to non‐zoo areas, while providing medical and veterinary benefits to zoo animals, employees and patrons.     

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.     

A Postzoo Future: Why Welfare Fails Animals in Zoos

ABSTRACT

Discussions on the welfare of nonhuman animals in zoos tend to focus on incremental improvements without addressing the underlying problem of captivity. But alterations to the conditions of zoo captivity are irrelevant for animals. Real zoo reform will involve working to completely change the landscape. We offer six necessary reforms to bring zoos into a more ethical future: (1) Shut down bad zoos, now; (2) stop exhibiting animals who cannot and never will do well in captivity; (3) stop killing healthy animals; (4) stop captive breeding; (5) stop moving animals around from one zoo to another; and (6) use the science of animal cognition and emotion on behalf of animals.     

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.     

Being Attractive Brings Advantages: The Case of Parrot Species in Captivity

Background

Parrots are one of the most frequently kept and bred bird orders in captivity. This increases poaching and thus the potential importance of captive populations for rescue programmes managed by zoos and related institutions. Both captive breeding and poaching are selective and may be influenced by the attractiveness of particular species to humans. In this paper, we tested the hypothesis that the size of zoo populations is not only determined by conservation needs, but also by the perceived beauty of individual parrot species assessed by human observers.

Methodology/Principal Findings

For the purpose of data collection, we defined four sets of species (40 parrots, 367 parrots, 34 amazons, 17 macaws). Then, we asked 776 human respondents to evaluate parrot pictures of the selected species according to perceived beauty and we analyzed its association with color and morphological characters. Irrespective of the species set, we found a good agreement among the respondents. The preferred species tended to be large, colorful, and long-tailed.

Conclusions/Significance

We repeatedly confirmed significant, positive association between the perceived beauty and the size of worldwide zoo population. Moreover, the range size and body size appeared to be significant predictors of zoo population size. In contrast, the effects of other explanatory variables, including the IUCN (International Union for Conservation of Nature) listing, appeared insignificant. Our results may suggest that zoos preferentially keep beautiful parrots and pay less attention to conservation needs.     

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.     

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.     

What Is the Future for Zoos and Aquariums?

ABSTRACT

Animal welfare concerns have plagued the professional zoo and aquarium field for decades. Societal differences remain concerning the well-being of animals, but it appears a shift is emerging. Scientific studies of animal welfare have dramatically increased, establishing that many previous concerns were not misguided public empathy or anthropomorphism. As a result, both zoo and aquarium animal welfare policy and science are now at the center of attention within the world’s professional zoos and aquariums. It is now possible to view a future that embraces the well-being of individual captive exotic animals, as well as that of their species, and one in which professional zoos and aquariums are dedicated equally to advancing both. Though the ethics of keeping exotic animals and animals from the wild in captivity are still a contentious subject both outside and even within the profession, this study argues. We argue that this path forward will substantially improve most zoo and aquarium animals' welfare and could significantly reduce societal concerns. If animal welfare science and policy are strongly rooted in compassion and embedded in robust accreditation systems, the basic zoo/aquarium paradigm will move toward a more thoughtful approach to the interface between visitors and animals. It starts with a fundamental commitment to the welfare of individual animals.     

Human–Animal Bonds Between Zoo Professionals and the Animals in Their Care

Some human‐animal relationships can be so positive that they confer emotional well‐being to both partners and can thus be viewed as bonds. In this study, 130 delegates at zoo research and training events completed questionnaires in which they were asked about their professional work in the zoo and whether they believed they had established bonds with any animals. They were also asked to indicate agreement or disagreement with several statements about human‐animal bonds. Results showed that many zoo professionals consider that they have established bonds with some of their animals; 103 respondents believed that they had a bond with at least one animal, and 78 of these identified that the bond was with a zoo animal. The most frequent bonds reported were with primates (n = 24) and carnivores (n = 28). Perceived benefits of these bonds to the respondents included both operational (animal easier to handle, easier to administer treatments to) and affective (sense of well‐being, enjoyment at being with the animal). Identifying benefits to the animals was more difficult. Most respondents identified similar benefits for their animals as for themselves, i.e. operational (animal responded more calmly, appeared less stressed) and affective (animal appeared to enjoy contact with respondent, seemed more content). This suggests that bonding between zoo professionals and their animals could have profound consequences for the management and welfare of the animals, not to mention the job satisfaction of the people involved. Zoo Biol 31:13;–26, 2012. © 2010 Wiley Periodicals, Inc.     

The historical development of zoo elephant survivorship

In the discussion about zoo elephant husbandry, the report of Clubb et al. (2008, Science 322: 1649) that zoo elephants had a “compromised survivorship” compared to certain non-zoo populations is a grave argument, and was possibly one of the triggers of a large variety of investigations into zoo elephant welfare, and changes in zoo elephant management. A side observation of that report was that whereas survivorship in African elephants (Loxodonta africana) improved since 1960, this was not the case in Asian elephants (Elephas maximus). We used historical data (based on the Species360 database) to revisit this aspect, including recent developments since 2008. Assessing the North American and European populations from 1910 until today, there were significant improvements of adult (≥10 years) survivorship in both species. For the period from 1960 until today, survivorship improvement was significant for African elephants and close to a significant improvement in Asian elephants; Asian elephants generally had a higher survivorship than Africans. Juvenile (<10 years) survivorship did not change significantly since 1960 and was higher in African elephants, most likely due to the effect of elephant herpes virus on Asian elephants. Current zoo elephant survivorship is higher than some, and lower than some other non-zoo populations. We discuss that in our view, the shape of the survivorship curve, and its change over time, are more relevant than comparisons with specific populations. Zoo elephant survivorship should be monitored continuously, and the expectation of a continuous trend towards improvement should be met.     

Maintaining the genetic health of putative Barbary lions in captivity: an analysis of Moroccan Royal Lions

The last representatives of the Barbary lion (Panthera leo leo), once numerous in North Africa but exterminated from the wild by the 1940s, are believed to be the captive lions descended from the Moroccan Royal Collection, numbering less than 90 animals in zoos worldwide. The genetic fitness of these captive “Royal Lions” may now be under threat since, although most zoos have avoided hybridisation with animals of other origin, no formal breeding programme currently exists and several institutions have halted breeding activities. This situation has arisen since the distinctiveness of Barbary lions and the representative status of Royal Lions remain inconclusive and definitive molecular studies have yet to be completed. Previously, in the 1970s, morphological and phenotypic traits were used to match Royal Lions and the historic Barbary lion and an ex situ breeding programme was initiated involving a number of selected “founder” animals. This paper outlines the status of the descendent population within zoos in Morocco and Europe, including all known pure-bred descendents from the Royal Palace collection. Founder representation is shown to be greater across European collections than the Moroccan collection. Breeding exchanges are recommended between institutions in order to improve genetic diversity and maintain the genetic health of the population and a studbook for European zoo animals has been developed to support this action. This analysis serves as a benchmark for guiding effective maintenance of the captive population, thereby allowing time to clarify the conservation value of Royal Lions and their relevance to North African ecology.