Activity budget and spatial distribution of Bennett's wallabies (Macropus rufogriseus) in open versus closed exhibit designs

Although many studies investigating the impacts of zoo exhibit designs on captive animals exist, none have been performed on how they influence the behavior and welfare of captive Bennett's wallabies (Macropus rufogriseus). Here, we assess the impact of exhibit design on the activity budget and spatial distribution of Bennett's wallabies. We compared animal behavior in two open exhibits (i.e. physical interaction between animals and visitors permitted) to two closed exhibits (i.e. physical interaction between animals and visitors prohibited). Behavioral data were collected using focal sampling, and spatial distribution was recorded on exhibit maps at regular time intervals. We found a significant increase in feeding and interactive behaviors in closed exhibits in comparison to open exhibits. However, other behaviors such as resting, locomotion, and vigilance did not vary with design. Functional use of space was similar between both designs; however, the effect of habituation may be relevant to consider in future studies. Although some support for visitor effects were present, our study provided no evidence for strong impacts of exhibit design on Bennett's wallaby welfare. Our study emphasizes the need for additional research into the impacts of how zoo environments affect Bennett's wallaby behavior and welfare.     

Social interaction analysis in captive orcas (Orcinus orca)

The management of socially complex species in captivity is challenging. Research on their social behavior improves our understanding of interactions in captive animals and captive‐group management. We conducted a detailed analysis of social relationships shown by the orcas kept at Loro Parque zoo and their tendency to reconcile after aggressive episodes. Affiliative interactions were the most frequent social activities compared to agonistic or sexual interactions. Within affiliative behaviors, we documented the pattern “gentle tongue bite”, where an animal touches the other's tongue with his teeth but does not bite it. Affiliative interactions between a specific pair of orcas occurred significantly more often than expected by chance, and together with low levels of agonistic interactions, indicated particular affinity between some individuals. The most frequently observed low‐level agonistic relationship was that of the two older males (Tekoa–Keto); however, they also showed frequent sexual and affiliative interactions. Sexual‐like behaviors (pursuit, mount, and penis between males) were found in both sexes. Finally, the observed corrected conciliatory tendency (31.57%) was within the range described for other primate and cetacean species. This study provides a systematic way to assess social interactions as well as conflict management strategies in cetaceans housed in zoos and zoo‐like facilities and may help to improve animal welfare and management of animals in controlled environments.     

Exoticism as a Mediator of Everyday Experiences of Nature: an Anthropological Exploration of Soundscape in Zoos

The increasing levels of stress entailed by contemporary urban lifestyles can lead to a greater desire to escape from cities. The restorative sense of ‘being away’ produced by natural environments has been substantially explored in greenspaces but little studied in zoos, which endeavour to immerse visitors in a local or exotic environment through both the visual environment and soundscape. We explore how soundscapes contribute to this sense of immersion through self-reflective interviews with 20 participants in two zoos in Paris (France). The zoo was perceived as a natural or a socially crowded area depending on the auditory context. Interestingly, focusing on the captive exotic animals seemed to make participants more aware of the more common birds around them in the zoo. By highlighting both, zoos could potentially increase awareness and care for urban biodiversity.     

Conceptual and methodological issues in the comparative study of collective group movements

In our commentary, we highlight several conceptual and methodological problems that have hampered broader integration of studies of collective group movements. Specifically, we argue that studies of captive animals should only be used to elucidate behavioural mechanisms. Moreover, the diversity of physical environments in which group movements occur as well as the social diversity of groups deserve more consideration in integrative studies. Furthermore, tests of predictions based on modelling studies are often hampered by the fact that models include variables that are difficult or impossible to measure in real animals. We also advocate the use of an empirical, rather than subjective establishment of operational definitions of group movements and the associated individual roles. Finally, we emphasize the utility of controlled experiments in the study of collective decision-making and group movements and encourage their wider application.     

Effects of early rearing experience on subsequent adult sexual behavior using domestic cats (Felis catus) as a model for exotic small felids

Zoo professionals generally believe that maternal rearing of zoo animals is preferable to human/nursery raising. The lack of consistent reproductive success in small captive exotic felids has been partially attributed to an excess of human-raised individuals. To investigate experimentally the effects of human/nursery rearing on adult sexual behavior, domestic cats were used as a model for small captive exotic felids. Three groups of female domestic cats were reared under three different conditions (intended to mimic typical zoo rearing situations) and then paired at sexual maturity with sexually experienced males. Cats in Condition 1 were Human-Raised Alone, i.e., had no physical or visual contact with con-specifics until sexual maturity; cats in Condition II were Human-Raised with a Sibling, i.e., had no physical or visual contact with any conspecifics except their respective sibling until sexual maturity; cats in Condition 3 were Maternally Raised with a female sibling, but had no other physical or visual contact with other conspecifics until sexual maturity. Individuals in Condition 3 copulated significantly more often than did the individuals in Condition 1. The individuals in Condition 1 were distinguished by the extreme aggression they displayed toward both the males with which they were paired and their human-caretakers. Data suggest that human-reared female cats are less likely to reproduce than are their maternally-reared counterparts. These results suggest that, whenever possible, nursery-raising of small exotic felids should be avoided.     

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.     

Behavior of the mayotte lemur,Lemur fulvus mayottensis,in captivity

A group of one male and two female Mayotte lemurs was observed at Chester Zoo, and their behaviors compared with published observations of wild populations of this and related forms of the brown lemur. It was found that the captive animals were active by both day and night, but that the pattern of activity was different from wild lemurs. The captive lemurs were less active than their wild counterparts and showed different timing of activity because of the feeding regimen at the zoo. The animals did not ignore the public at the zoo, but, on the contrary, directed some behaviors at the zoo visitors, particularly if the zoo visitors attempted to interact with the lemurs; under these conditions there was also an increase in the movements of the lemurs in the cage. Levels of aggression in the zoo lemurs were higher than those reported for wild populations, and aggression appeared to occur predominantly in the birth season. Levels of affiliative behaviors, particularly allogrooming, were comparable with those in the wild. Olfactory behaviors such as scent marking and anogenital sniffing also showed seasonal peaks and again appeared to occur at higher rates than in the wild.     

Managerial strategies in the captive propagation of endangered species

A captive propagation manager, committed to the welfare of captive populations of exotic animals, must often make decisions that are risky to individual animals. Innovative decisions that place animals at risk are essential to the progress of captive propagation. Such decisions must be grounded thoroughly on peer consultation, the scientific and zoo literature, and where possible on original applied research targeted specifically to the procedure in question. The management of two closely spaced births in a gorilla group is provided as an example.     

Space use selectivity by chimpanzees and gorillas in an indoor-outdoor enclosure

Understanding the relationship between physical environments and nonhuman primate behavior is a key element for effective care and management in a range of settings. The physical features of the captive environment, including not only gross useable space but also environmental complexity, can have a significant influence on primate behavior and ultimately, animal welfare. But despite this connection, there remains relatively little conclusive data on how captive primates, especially great apes, use the spaces provided to them, especially in modern, indoor-outdoor enclosures that have become more prevalent in recent years. In this study, we used four years of detailed data on where 23 great apes (chimpanzees and gorillas) positioned themselves within a modern, indoor-outdoor zoo enclosure to determine not only how the apes utilized their space but also how access to outdoor areas affected their spatial selectivity. We found that both species used relatively little of their available space: chimpanzees and gorillas spent half their time in only 3.2 and 1.5% of their useable three-dimensional space, respectively. Chimpanzees utilized the outdoor space more than gorillas, but access to the outdoors did not affect space selectivity in the indoor area for either species. Although both species of ape were highly selective in their space use, consideration should be given to the importance of providing the choice to locate in a variety of spaces, including outdoor areas. These data represent an extremely detailed account of space selectivity by great apes in an indoor-outdoor environment and have substantial implications for future facility design and captive primate management.     

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.     

The Impact of Cognitive Testing on the Welfare of Group Housed Primates

Providing cognitive challenges to zoo-housed animals may provide enriching effects and subsequently enhance their welfare. Primates may benefit most from such challenges as they often face complex problems in their natural environment and can be observed to seek problem solving opportunities in captivity. However, the extent to which welfare benefits can be achieved through programmes developed primarily for cognitive research is unknown. We tested the impact of voluntary participation cognitive testing on the welfare of a socially housed group of crested macaques (Macaca nigra) at the Macaque Study Centre (Marwell Zoo). First, we compared the rate of self-directed and social behaviours on testing and non-testing days, and between conditions within testing days. Minimal differences in behaviour were found when comparing testing and non-testing days, suggesting that there was no negative impact on welfare as a result of cognitive testing. Lipsmacking behaviours were found to increase and aggressive interaction was found to decrease in the group as a result of testing. Second, social network analysis was used to assess the effect of testing on associations and interactions between individuals. The social networks showed that testing subjects increased their association with others during testing days. One interpretation of this finding could be that providing socially housed primates with an opportunity for individuals to separate from the group for short periods could help mimic natural patterns of sub-group formation and reunion in captivity. The findings suggest, therefore, that the welfare of captive primates can be improved through the use of cognitive testing in zoo environments.     

The utility of captive animals in actualistic research: A geometric morphometric exploration of the tooth row of Alligator mississippiensis suggesting ecophenotypic influences and functional constraints

Captive broad snouted crocodylians are generally thought to have wider, shorter rostra than their wild counterparts. Interpreted to reflect morphological change in response to the conditions of captivity, this qualitative pattern could affect the utility of these animals in a variety of fields of research. However, due to relative ease of access and availability of life history data, captive animals are often utilized in actualistic research. Thus, this issue should be addressed in more detail. Here we explore snout shape variation between captive and wild members of Alligator mississippiensis using two‐dimensional (2D) morphometric techniques. Several landmark schemesare used to assess the utility of different aspects of morphology in distinguishing the groups. While statistical analyses consistently differentiated between the groups, the area of morphospace occupied by wild members of A. mississippiensis generally overlapped with the larger area encompassing the captive specimens. This indicates that the captive condition is not as uniform as previously thought and instead encompasses a large spectrum of morphologies, ranging from the stereotypical broad, shortened snouts to outlines that are indistinguishable from the wild morphotype. These results align well with the interpretation that this change reflects an extreme example of ecophenotypy, since ranched, farmed, or zoo organisms are held in an array of enclosures, ranging from indoor, climate controlled pens to outdoor, more natural areas. This variation in environments should be reflected in different reactions to the animals' surroundings, resulting in a broad spectrum of morphotypes. While wild specimens are still preferred, especially for fine scale analyses, these results indicate that not all captive members of A. mississippiensis exhibit the extreme morphological alterations often cited in the literature. Weighing the conditions in which the animals are held and exploring the possibility of morphological differences against the benefits of using captive specimens should be part of any actualistic study. J. Morphol. 277:866–878, 2016. © 2016 Wiley Periodicals, Inc.     

Speichelforschung im Zoo - Eine Hilfe zur artgemäßen Fütterung von Tierarten mit besonderer Nahrungsanpassung

Between 2008 and 2010 the Zoological gardens in Rheine, Stuttgart, Karlsruhe, Cologne and Zurich took part in a research project initiated by scientists of the Institute of Animal Science, University of Bonn. Saliva was collected from various zoo animals to determine certain dietary adaptations on enzymatic and physiological levels that might explain or change our current understanding of animal nutrition and the feeding in zoo environments. The interest was primarily focused on species with specialized nutritional needs or fermentation strategies such as geladas, chimpanzees, camels and zebras. The work produced highly valuable data especially on geladas, which, despite from their adaptation to grass diet, revealed to have the enzymatic precondition (salivary amylase) to use starch-rich food items very effectively. Therefore, to prevent obesity in captive geladas, the reduction of starchy food in their daily rations is mandatory. Finally, saliva sampling is an easy, cost-effective and non-invasive procedure, the use of which is both practical and attractive in a zoo environment. In the future, the world-wide emerging field of salivary research might give birth to new applications of saliva as a tool to detect biomarkers of physiology and diseases in zoo animals.     

Similarities and differences in activities and agonistic behavior of male Eastern grey kangaroos (Macropus giganteus) in captivity and the wild

The behavior of free-ranging and captive Eastern grey kangaroos Macropus giganteus, was observed by the same observers, with similar methods and under similar vegetational/climatic conditions in a 4.2-ha enclosure at Neuwied Zoo, Germany and at Grampians National Park, Victoria, Australia. Data were collected from a zoo group of 56 animals and a free-ranging mob of 50 to 60 animals. Males were individually identified and observed: 3 large males, 9 medium males, and 10 small males in the zoo, and 8 large, 9 medium, and approximately 10 small males in the National Park were present. Activities in both situations were very similarly distributed: Feed took up less time in the zoo, resting was almost similar in both situations, alert behavior was significantly different for small and medium males, locomotor activities were similar in large males and females, autogrooming occurred significantly more in the zoo only for females. Frequencies of social interactions were slightly greater for large males and females in the zoo. Agonistic behavior in males was more frequent in the zoo situation, except for ritualized fights. Sequences of agonistic behavior were more predictable in the zoo. No differences in escalation tendencies toward potentially injurious fighting could be found. Zoo Biol 19:529-539, 2000. Copyright 2000 Wiley-Liss, Inc.     

The Effect of Fission–Fusion Zoo Housing on Hormonal and Behavioral Indicators of Stress in Bornean Orangutans (Pongo pygmaeus)

The welfare of captive animals could be improved if zoos were to place more emphasis on their species-specific needs. In the wild, orangutans live in a fission–fusion social system and have a semisolitary lifestyle. However, most zoos keep orangutans in permanent groups, which may be stressful for them. Apenheul Primate Park in Apeldoorn, Netherlands, houses 14 Bornean orangutans in a simulated fission–fusion social system. To assess how this housing system affects indicators of stress, we measured fecal glucocorticoid metabolites (fGCM) and determined proportions of self-directed behavior (scratching and autogrooming). We compared fGCM concentrations of the Apenheul animals to those of zoo orangutans kept in permanent groups. In addition, we tested the effect of group size, visitor number, sex, age, and change of group composition on fGCM concentrations and proportions of self-directed behavior in the Apenheul orangutans. In contrast to Bornean orangutans housed in permanent groups, we did not find a group size effect on fGCM or on self-directed behavior in Apenheul’s fission–fusion housing system. In addition, fGCM concentrations in Apenheul orangutans increased significantly with visitor numbers. Visitor number also affected proportions of self-directed behavior, and mean proportions of scratching were positively correlated with mean values of fGCM concentrations. Although these results suggest that the fission–fusion housing system in Apenheul reduces the group size effect leading to social stress in Bornean orangutans, they also show that visitors are an important factor that needs to be mitigated if the well-being of captive primates and other zoo animals is to be improved.     

Comparative study on the growth of juvenile Galapagos giant tortoises (Geochelone nigra) at the Charles Darwin Research Station (Galapagos Islands,Ecuador) and Zoo Zurich (Zurich,Switzerland)

In this study, the growth rates of a group of Galapagos giant tortoises raised in their natural habitat at the Charles Darwin Research Station (CDRS; Galapagos Islands, Ecuador) and a group of captive‐bred specimens (Zoo Zurich, Zurich, Switzerland) were compared for the first time. A great discrepancy in growth rates was observed after the first year. When the animals were 4 years old, the carapace in the Zurich specimens was approximately twice as long as that in the CDRS tortoises, and the Zurich animals weighed approximately 10 times more than the CDRS animals. The zoo diet was modified by a reduction in nutrients and an increase in fiber to produce a more natural growth rate. Zoo Biol 23:177‐183, 2004. © 2004 Wiley‐Liss, Inc.     

Preference for structural environmental features in captive lowland gorillas (Gorilla gorilla gorilla)

Increased interest in the behavioral effects of captive environments and advances in zoo design have resulted in a proliferation of “naturalistic” animal habitats. Although scientists have demonstrated that such exhibits have some positive effects on behavior, very little is known about the complex relationships between these specialized environments and behavior. This study sought to determine preferences for structural environmental features, such as slope and trees, exhibited by captive lowland gorillas (Gorilla gorilla gorilla). An average of 496 location scans were collected on each of 23 gorillas, housed in 6 groups. The results indicate that enclosure usage was significantly associated with the features of slope, nearness to holding facility, and presence of environmental components additional to substrate (e.g., tree or rock). In particular, areas with flat ground that were near the holding building and that included at least one component additional to substrate were preferred by all animals. © 1993 Wiley-Liss, Inc.     

Use of RAPD-PCR-analysis of cellular DNA for the evaluation of genetic polymorphism and subspecies diagnostics of the Far Eastern leopard Panthera pardus orientalis]

Genetic polymorphism in the Far-Eastern leopard subspecies Panthera pardus orientalis was examined by RAPD-PCR analysis of total cellular DNA. Primers diagnostic for the leopard subspecies were detected. These primers can be used for differentiating wild-living animals from those kept in captivity and distinguishing different breeding lines. Genetic diversity was shown to be lower in animals from the zoo (D = 0.058) and higher in a natural population (D = 0.137). Two lines of the Persian subspecies were genetically closest (D = 0.042), and the Persian and Far-Eastern subspecies represented by wild animals, genetically most remote (D = 0.274). The level of genetic divergence of the Persian subspecies and Far-Eastern subspecies (zoo animals) was lower (D = 0.108) than between representatives of the Persian subspecies from the captive and natural population (D = 0.220). On the basis of analysis of relatedness, performed using NTSYS and PHYLIP software packages, the possibility cannot be excluded that some P. p. orientalis animals from the zoo have a hybrid origin and may be assigned to another Far-Eastern subspecies.     

Variables influencing the origins of diverse abnormal behaviors in a large sample of captive chimpanzees (Pan troglodytes)

The developmental origin of abnormal behaviors is generally associated with early rearing environments that lack sufficient physical and sensory stimulation. However, other factors should also be considered. A large sample of captive chimpanzees (128 males and 140 females) was surveyed for the presence or absence of 18 abnormal behaviors. Origin variables included the subject's source (zoo, pet, performer, or laboratory), rearing (mother‐ or hand‐reared), and sex. Animals were assessed while held at the Primate Foundation of Arizona, University of Texas M. D. Anderson Cancer Center, or White Sands Research Center. There was a confound among origin variables; more hand‐reared animals than expected were from laboratories. Logistic regression tested the relationship of rearing and source, with sex as a secondary predictor variable, to each of the abnormal behaviors. There was no clear association between any abnormal behavior and source. However, for coprophagy, relative to animals from the laboratory, zoo animals tended to show a higher prevalence, while performers tended to show a lower prevalence (when rearing and sex were controlled). Rocking and self‐sucking were significantly more likely in hand‐reared animals. Coprophagy and depilation of self were significantly more likely in mother‐reared animals. When rearing and source were statistically controlled, the only significant sex difference was a higher prevalence of coprophagy in females and a higher prevalence of rocking in males. In a second, smaller sample of 25 males and 33 females from Southwest Foundation for Biomedical Research, no significant sex association was found for coprophagy, urophagy, rocking, or self‐depilation. In this second sample, coprophagy was also significantly more likely in mother‐reared than hand‐reared subjects. The association of some abnormal behaviors with mother‐rearing suggests that some form of social learning may be involved in the origin of some of these behavior patterns. This indicates that some abnormal behaviors may not be always be indicative of reduced psychological well‐being in captive chimpanzees. Am. J. Primatol. 48:15–29, 1999. © 1999 Wiley‐Liss, Inc.