Zoo Animal Welfare: The Human Dimension

ABSTRACT

Standards and policies intended to safeguard nonhuman animal welfare, whether in zoos, farms, or laboratories, have tended to emphasize features of the physical environment. However, research has now made it clear that very different welfare outcomes are commonly seen in facilities using similar environments or conforming to the same animal welfare requirements. This wide variation is almost certainly due, at least in part, to the important effects of the actions of animal care staff on animal welfare. Drawing mostly on the farm animal literature, we propose that this “human dimension” of animal welfare involves seven components: (1) positive human–animal interaction, (2) consistency and familiarity of keepers, (3) treating animals as individuals and taking account of their personalities, (4) the attitudes and personalities of keepers, (5) the keepers’ knowledge and experience, (6) the keepers’ own well-being, and (7) the influence of facility design on how keepers and others interact with the animals. We suggest that attention to these human factors provides major scope for improving the welfare of animals in zoos.     

A Comparison of Zoo Animal Behavior in the Presence of Familiar and Unfamiliar People

As recorded in domestic nonhuman animals, regular interactions between animals in zoos and keepers and the resulting relationship formed (human–animal relationship [HAR]) are likely to influence the animals' behaviors with associated welfare consequences. HAR formation requires that zoo animals distinguish between familiar and unfamiliar people. This ability was tested by comparing zoo animal behavioral responses to familiar (routine) keepers and unfamiliar keepers (participants in the “Keeper for the Day” program). Study subjects included 1 African elephant (Loxodonta Africana), 3 Rothschild's giraffes (Giraffa camelopardalis rothschildi), 2 Brazilian tapir (Tapirus terrestris), and 2 slender-tailed meerkats (Suricata suricatta). Different behavior was evident and observed as decreased avoidance behavior toward familiar keepers (t₇ = 6.00, p < .001). This finding suggests the zoo animals have a lower level of fear toward familiar keepers. Keeper familiarity did not significantly affect any other behavioral measure. This finding suggests that in the current study, unfamiliar keeper presence did not appear to have detrimental effects. Furthermore, unfamiliar keeper–animal interactions could provide an increased number of positive human–animal interactions and potentially enhance animal welfare.     

Technology at the Zoo: The Influence of a Touchscreen Computer on Orangutans and Zoo Visitors

A computer‐controlled touchscreen apparatus (hereafter referred to as “touchscreen”) in the orangutan exhibit at Zoo Atlanta provides enrichment to the animals and allows cognitive research to take place on exhibit. This study investigated the impact of the touchscreen on orangutan behavior and visibility, as well as its impact on zoo visitors. Despite previous research suggesting that providing a single computer system may negatively affect orangutan behavior, there was not a significant increase in aggression, stereotypic, or distress‐related behaviors following the activation of the on‐exhibit touchscreen. We also investigated the possibility that zoo visitors may be negatively affected by technology because it deviates from naturalism. However, we did not find a change in stay time or overall experience rating when the computer was turned on. This research was the first to assess visitor attitudes toward technology at the zoo, and we found that visitors report highly positive attitudes about technology for both animals and visitors. If subjects visited the exhibit when the computer was turned on, they more strongly agreed that orangutans benefit from interacting with computerized enrichment. This study is the first investigation of an on‐exhibit touchscreen in group‐housed apes; our findings of no negative effects on the animals or zoo visitors and positive attitudes toward technology suggest a significant value of this practice. Zoo Biol 31:27;–39, 2012. © 2011 Wiley Periodicals, Inc.     

Food for Thought: Assessing Visitor Comfort and Attitudes toward Carcass Feeding at the ABQ BioPark Zoo

Enrichment is a key to keeping animals in zoos healthy and stimulated. For carnivores, the practice of feeding vertebrate animal carcasses, like those of goats or deer, or whole body prey animals like chickens or rabbits, can be an effective form of enrichment. While it is beneficial for animal care, carcass feeding may also be off-putting to some visitors. This research aimed to address this concern by describing the attitudes and comfort levels of visitors who viewed carcass feeding in three exhibits at the ABQ BioPark Zoo in Albuquerque, New Mexico: spotted hyena (Crocuta crocuta), Tasmanian devil (Sarcophilus harrisii), and African painted dog (Lycaon pictus). Results showed that visitors stayed at exhibits longer when a carcass was introduced and reported feeling generally comfortable and at ease while viewing carcass feeding. Findings also showed that visitors felt carcass feeding was beneficial to animal care and welfare.     

Sarcocystosis among Wild Captive and Zoo Animals in Malaysia

Sarcocystis sp. infection was investigated in 20 necropsied captive wild mammals and 20 birds in 2 petting zoos in Malaysia. The gross post-mortem lesions in mammals showed marbling of the liver with uniform congestion of the intestine, and for birds, there was atrophy of the sternal muscles with hemorrhage and edema of the lungs in 2 birds. Naked eye examination was used for detection of macroscopic sarcocysts, and muscle squash for microscopic type. Only microscopically visible cysts were detected in 8 animals and species identification was not possible. Histological examination of the sections of infected skeletal muscles showed more than 5 sarcocysts in each specimen. No leukocytic infiltration was seen in affected organs. The shape of the cysts was elongated or circular, and the mean size reached 254 × 24.5 µm and the thickness of the wall up to 2.5 µm. Two stages were recognized in the cysts, the peripheral metrocytes and large numbers of crescent shaped merozoites. Out of 40 animals examined, 3 mammals and 5 birds were positive (20%). The infection rate was 15% and 25% in mammals and birds, respectively. Regarding the organs, the infection rate was 50% in the skeletal muscles followed by tongue and heart (37.5%), diaphragm (25%), and esophagus (12.5%). Further ultrastructural studies are required to identify the species of Sarcocystis that infect captive wild animals and their possible role in zoonosis.     

Visitor behavior in zoos: A review

Abstract

Visitors are integral components of zoological parks and their importance has led to a research area devoted to understanding the people–zoo relationship. This paper reviews, and provides a point of entry into, the literature relating to visitor research in zoos. The field emerged relatively recently and is diverse and interdisciplinary (it shares common ground with sociology, education, psychology, zoology, and other academic disciplines). Several areas can be identified in the literature (audience analysis, circulation and orientation, exhibit evaluation, and interactions with animals), and these areas have revealed visitors' demographic and behavioral characteristics, people's behavioral responses to endogenous and exogenous factors, the impact of exhibit design, and visitors' movements around zoos. Limitations of existing work include independence between research areas, lack of international studies, limited generalizability of results, and the minority status of the field. Therefore, suggestions for future work include integrating different research areas, more research from outside Europe and America, and increased interaction within the visitor research community.     

Evaluation of Factors Affecting Emotional Responses in Zoo Visitors and the Impact of Emotion on Conservation Mindedness

Creating experiences for visitors that increase their biological knowledge and inspire conservation mindedness is a critical task for zoos and aquariums. A growing body of literature suggests that emotional stimulation is affected by characteristics of both the visitor and the visitor's experiences and is important for learning and inspiring pro-environmental sentiment. In this study we explored relationships between emotional experience, the factors that influence it, visitors' predispositions toward nature, and their reports of conservation mindedness after viewing three carnivore exhibits at the Bronx Zoo, USA. We surveyed visitors after they viewed tigers, African wild dogs, and spotted hyenas during baseline conditions or when the animals were given environmental enrichment to stimulate natural behavior and activity. We asked visitors to report their predispositions toward nature, the extent of positive emotional experiences they had while viewing the animals, and how the experience affected their conservation mindedness. Environmental enrichment significantly increased animal behavioral diversity, particularly for African wild dogs, and contributed to visitors reporting having had an up-close encounter with the animals, both of which affected the strength of positive emotional experiences at the exhibits. The extent of eye contact with the animal and the animal species also significantly affected emotional responses. Women reported stronger emotional experiences than men, however younger adults did not experience stronger positive emotional responses than older participants. Visitors' predispositions toward nature and emotional responses were significantly correlated. Strong predispositions toward nature and emotional experiences produced significantly stronger reports of conservation mindedness in visitors as a result of their experience at the exhibit. These findings have implications for animal husbandry, exhibit design, education, and outreach efforts for zoos.     

It's a sign: Animal welfare and zoo type are predictors of animal identification signage usage and quality at zoo exhibits

Conservation education programs are listed as priority actions for almost every threatened species on the International Union for Conservation of Nature Red List. Zoos play an important role in delivering such programs, yet evidence of zoo education in many non-western countries is limited. Here, we evaluate animal identification signage prevalence and quality at zoo exhibits and investigate whether animal welfare, zoo type (accredited, government, and private), admission fee, zoo size, and proximity to urban centers are influencing factors. We used hornbills (Bucerotidae) as a model taxon, surveyed hornbill signage, and conducted welfare assessments of hornbill exhibits. We developed scoring frameworks and applied content analysis to analyze signage quality. Our results show that out of 18 zoos that displayed hornbills, 15 had hornbill signage. However, of the 106 hornbill exhibits in these zoos, 33% had no signage. We also found that signage presence or absence at individual zoos and signage quality is strongly correlated with animal welfare quality. Zoo type is a key factor in predicting signage and welfare quality, with accredited zoos scoring highest for both signage and welfare, followed by government and private zoos. Private zoos charged higher admission than other zoo types, and zoo size and proximity to urban centers did not influence signage or welfare scores. Overall, we conclude that in our study, signage usage and quality are inadequate, highlighting the importance of compliance with robust zoo standards to improve education and welfare within zoos to support global conservation goals.     

Unraveling the Complexity of the Zoo Community: Identifying the Variables Related to Conservation Performance in Zoological Parks

Zoological parks make up a highly heterogeneous community. Ranging from small collections at shopping malls to highly developed bioparks, their contribution to conservation is expected to vary enormously. Although several studies have focused on assessing such contribution, the parameters used frequently do not apply when considering more modest zoos. The goals of this study are to determine, within the wide range of zoos, which type tend to fulfill the conservation mission of modern zoos and to identify the variables associated to their conservation performance. We used the requirements demanded by the European Community Zoos Directive 1999/22/EC, relating to the keeping of wild animals in zoological parks, to assess conservation performance in 72% of officially registered Spanish zoos. Sampled zoos were classified into groups according to their common characteristics, and then the variables related to how they met each of the Directive's requirements in the groups were assessed. We found that private zoological parks with large zoological collections, located within metropolitan areas, and members of a zoo association tended to fulfill the requirements. Being a member of a zoo association was the variable that better explained fulfillment of the requirements among the evaluated zoos. Data revealed that zoos not meeting any requirement were few, although those meeting all of them were not frequent. The requirement related to adequate record keeping showed the lowest level of fulfillment. We discuss the implications of our results and propose measures of change in order to promote the contribution of zoos to biodiversity conservation. Zoo Biol 31:55;–70, 2012. © 2011 Wiley Periodicals, Inc.     

Reproduction of varanid lizards (Reptilia: Squamata: Varanidae) at the Bronx Zoo

Captivity provides many opportunities for studying the reproductive biology of varanid lizards (Family: Varanidae; genus: Varanus). This article presents reproductive data for 12 varanid species maintained in captivity at the Bronx Zoo between 1977 and 2010. Five species, V. prasinus, V. beccarii, V. melinus, V. mertensi, and V. ornatus have successfully reproduced at the zoo, for which clutch, incubation, and hatchling data are presented, and compared with previously published values. Clutch, incubation, and hatchling measurements typically fell within the known ranges for each species, or represent minor range extensions. V. mertensi was the only species that reproduced seasonally (χ(2) = 9.061, P = 0.029). Five species multiclutched; individual V. mertensi and V. prasinus females produced as many as four clutches per year. The shortest intervals between successive clutches observed for V. kordensis (61 days), V. melinus (77 days), V. mertensi (51 days), and V. prasinus (68 days) represent the shortest known values for each species. Relative clutch mass (RCM) ranged from 0.187 to 0.437. A mean RCM of 0.370 ± 0.092 for V. prasinus is substantially higher than previously published values for the species. These results illustrate that when maintained under favorable conditions in captivity, some varanids are capable of remarkably high fecundities, rapid reproductive turnover rates, and sizeable maternal investments. Periodicals, Inc.     

Isolation of Salmonella from environmental samples collected in the reptile department of Antwerp Zoo using different selective methods

AIMS: To evaluate the environmental spread of Salmonella strains in the reptile department of Antwerp Zoo and to compare different isolation methods for Salmonella. METHODS AND RESULTS: One hundred environmental samples were collected in the service sections and public spaces of the reptile department. After pre-enrichment in buffered peptone water (BPW), selective enrichment was performed in Rappaport Vassiliadis Single Component Enrichment Broth (RVS), Selenite Cystine Broth (SEL) and Mueller Kauffman Tetrathionate Broth (MKTTn). Subculturing on Modified Semisolid Rappaport-Vassiliadis (MSRV) Medium, and the combined use of immunomagnetic separation (IMS) and RVS was evaluated. The isolation media used were Hektoen Enteric Agar (HE), Phenol Red Brilliant Green Agar (BG) and Xylose Lysine Decarboxylase Agar (XLD). Salmonella strains were found in 47 samples (47.0%). Most isolations were made on HE after combined IMS/RVS enrichment. Sixty-six Salmonella strains were serotyped, 29 belonged to Salmonella enterica ssp. enterica (I), 3 to ssp. salamae (II), 29 to ssp. arizonae or diarizonae (IIIa/b), 4 to ssp. houtenae (IV) and 1 strain showed autoagglutination. In addition, a 10-year survey (1995-2004) of Salmonella serovars isolated from reptiles at Antwerp Zoo is presented. CONCLUSIONS: A high prevalence of Salmonella strains was noted in the service sections of the reptile department. Only a few isolations were made in the public spaces. Selective enrichment in RVS was the most efficient. In combination with IMS, this method gave an even higher isolation rate than the International Standard method (ISO 6579:2002). SIGNIFICANCE AND IMPACT OF THE STUDY: This study confirms the importance of reptiles as spreaders of Salmonella in their surroundings. The possible infectious risks for zoo personnel and visitors are evaluated. Improved laboratory protocols for the isolation of Salmonella from the environment are suggested.     

Gum feeder as environmental enrichment for zoo marmosets and tamarins

Tamarins and marmosets are small-bodied social callitrichines. Wild callitrichines feed on exudates, such as sap and gum; particularly, marmosets are mainly gummivores, while tamarins consume gums only occasionally and opportunistically. Zoo marmosets and tamarins are usually provided with gum arabic as an alternative to the exudates normally found in the wild. The aim of this study was to evaluate the effects of a gum feeder on the behavior and well-being of four zoo-managed callitrichines. We studied four cotton-top tamarins (Saguinus oedipus), four red-handed tamarins (S. midas), two pygmy marmosets (Cebuella pygmaea), and three Geoffroy's marmosets (Callithrix geoffroyi) housed at Parco Natura Viva (Italy). We conducted the study over two different periods, a baseline (control, without the gum feeder) and then a gum feeder (when the gum feeder was provided) period. We used continuous focal animal sampling to collect behavioral data, including durations of social and individual behaviors. We collected 240 min of observations per period per study subject, with a total of 3,120 min for all the subjects in the same period and of 6,240 min in both periods. We analyzed data by using nonparametric statistical tests. First, we found that the gum feeder promoted species-specific behaviors, such as exploration, and diminished self-directed behaviors, suggesting an enriching effect on tamarin and marmoset behavior. Moreover, in red-handed tamarins, the provision of the gum feeder reduced the performance of self-directed and abnormal behavior, specifically coprophagy. These results confirm that gum feeders are effective foraging enrichment tools for zoo marmosets and tamarins.     

The selection of introduced sounds to improve the soundscape in the public spaces

The purpose of introducing sounds is to afford a comfortable acoustic environment and to design good soundscapes. This study aims at rating the preference of subjects for the introduced sounds suitable to the public spaces and also investigates the methodology to select the sounds by subjective and objective procedures. Seventeen kinds of the introduced sounds were evaluated with nine adjectives in the presence of visual location information. Also, adequate sound levels were calculated by adjusting the volume of introduced sounds in the presence of the actual background sounds of locations and visual information. The concept of harmony with the surroundings was reviewed by analyzing the correlation among 9 adjectives which express introduced sounds. And the effectiveness of existed sound quality index was analyzed so as to select the introduced sounds quantitatively. By the evaluation of the adequate level of the introduced sounds, it is proposed that the lower introduced sound level would be better for the noisy circumstances.     

The effects of olfactory stimulation on the behavior of captive ring‐tailed lemurs (Lemur catta)

Ring‐tailed lemurs reside in many animal collections worldwide. Lemur welfare may be a cause of concern due to some captive individuals exhibiting stereotypic behavior. Despite these concerns, there has been little exploration of methods of environmental enrichment for ring‐tailed lemurs. Olfactory stimulation can enhance captive animal welfare by encouraging species‐typical behaviors, enhancing behavioral diversity, and decreasing stereotypic behaviors. We aimed to investigate the effects of olfactory stimulation via lavender, peppermint, coconut, and prey odor upon the behavior of eight captive ring‐tailed lemurs. We exposed the lemurs to six individual odor conditions (odor control, novel object control, lavender, peppermint, coconut, and Morio worms) and observed them for 4 hr a day for 3 days with an intervening period of 4 days between conditions. We recorded the lemurs’ behavior under each condition using instantaneous scan sampling. We found significant effects of olfactory stimulation on the ring‐tailed lemurs’ behavior in the initial analysis but these did not survive correction for multiple testing. Overall, while our findings are suggestive of a general effect of olfactory stimulation on the captive ring‐tailed lemurs they did not indicate a marked influence of olfactory condition. However, further investigation with a larger sample size and more biologically relevant odors may be beneficial to fully examine potential effects of olfactory stimulation in captive lemurs.     

Intestinal parasitism—protozoa and helminths—in primates at the Barcelona Zoo

Abstract: The faunistic results regarding intestinal parasitism by protozoa and helminths in 21 primate species (three Cebidae, thirteen Cercopithecidae, one Hylobatidae, one Lemuridae, three Pongidae) are reported. The primate species were housed in four separate galleries. Six faecal samples of each host species were subjected to coprological analysis. Fifteen parasite species were detected: 11 protozoa (Entamoeba coli, E. chattoni, E. hartmanni, Iodamoeba bütschlii, Endolimax nana, Giardia intestinalis, Chilomastix mesnilii, Enteromonas hominis, Trichomonas intestinalis, Balantidium coli, and Blastocystis hominis) and 4 helminths (Ancylostoma sp., Strongyloides fuelleborni, Strongyloides sp., and Trichuris trichiura). The results reveal certain parasitic similarities between host species housed in the same gallery; however, these primate species do not always carry identical parasite species.