Zoo Playgrounds: A Source of Enrichment or Stress for a Group of Nearby Cockatoos? A Case Study

There is increasing evidence that in some circumstances, zoo visitors may be aversive stimuli to nonhuman animals housed in zoos. Yet, most previous research has focused on primates with little attention given to numerous other species who are housed in zoos. The focus animal of this project was the cockatoo, a species who has received minimal attention in zoo-based research. Furthermore, although the influence of the zoo setting has become increasingly important in visitor effect studies, this is the 1st study to quantify the effect of activity at a children's playground on zoo animals. There was an investigation on the effect of a zoo playground on the behavior of citron-crested and Moluccan cockatoos (Cacatua sulphurea citrinocristata and Cacatua moluccensis), as well as the effect of children standing in front of the birds' aviaries. The results showed that in some circumstances, the Moluccan cockatoos retreated from visitors, while the citron-crested cockatoos did not retreat from visitors and became more social in the presence of visitors. These findings highlight the importance of careful selection of species and individual animals to be housed near zoo playgrounds.     

mtDNA indicates profound population structure in Indian tiger (Panthera tigris tigris)

We analyzed mtDNA polymorphisms (parts of control region, ND5, ND2, Cytb, 12S, together 902 bp) in 59 scat and 18 tissue samples from 13 Indian populations of the critically endangered Indian tiger (Panthera tigris tigris), along with zoo animals as reference. Northern tiger populations exhibit two unique haplotypes suggesting genetic isolation. Western populations from Sariska (extinct in 2004) and Ranthambore are genetically similar, such that Ranthambore could serve as a source for reintroduction in Sariska. Zoo populations maintain mitochondrial lineages that are rare or absent in the wild.     

Genetic differentiation of the African dwarf crocodile Osteolaemus tetraspis Cope, 1861 (Crocodylia: Crocodylidae) and consequences for European zoos

The endangered African dwarf crocodile Osteolaemus tetraspis is distributed in Central and Western Africa. Conventionally, two subspecies were distinguished: Osteolaemus tetraspis tetraspis and Osteolaemus tetraspis osborni. The taxonomic significance of diagnostic morphological characters is still being discussed and the existence of additional species in the Osteolaemus group remains unclear. Recent molecular studies suggest the existence of three allopatric species in the genus Osteolaemus. These results supported a division of the dwarf crocodile into a Congo Basin form (O. osborni), an Ogooué Basin form (O. tetraspis), and a third separate evolutionary lineage from Western Africa. Several European zoos host African dwarf crocodiles. For reasons of conservation and possible reintroduction, it is important to clarify provenance of these zoo animals. Therefore, we conducted molecular and phylogenetic analyses of three mitochondrial and two nuclear gene sequences with all available samples from European zoos and museums. We also estimated the origin of the zoo animals by comparing sequences of wild animals and museum samples of known provenance. Our study strongly supports three distinct lineages of Osteolaemus as recently postulated, but also reveals a fourth evolutionary lineage. We demonstrate that, of the European zoo animals sampled, only one dwarf crocodile corresponds to the Congo Basin form (O. osborni) whereas the majority of individuals correspond to the three other forms. Four zoo animals belong to the new fourth group; but their provenance is still unresolved. The origin of these animals is probably located in an African region from which no wild animal samples are currently available. Further investigations and sampling of other regions should be completed to clarify the identity of this fourth lineage. We found potential hybrids from European zoological gardens using nuclear DNA sequences. The European Studbook will use these results for further breeding programmes to keep genetically suitable ex-situ populations as reassurance colonies for prospective reintroduction into African countries.     

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.     

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.     

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.     

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.     

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.     

Measuring the Strength of Human–Animal Bonds in Zoos

Repeated interactions within individual human and animal dyads can lead to the establishment of human–animal relationships (HARs), which may vary in quality from good to bad, defined in terms of the positivity (e.g., friendly contact, play) or negativity (e.g., aggression) of the interactions on which they are based. Particularly good HARs can be regarded as Human– Animal Bonds (HABs) if they are reciprocal and promote wellbeing in both parties. Although there is extensive evidence of the effects of HARs in agricultural animals and HABs in companion animals, there has been less investigation of these relationships in zoos, even though the development of HARs/HABs between zoo animals and their keepers could have important consequences for the welfare of both. Here we apply a modified version of the Lexington Attachment to Pets Scale (LAPS) in a zoo setting to quantify the strength of attachment of a sample of 22 keepers to the animals in their care at the zoo (ZA), in comparison with their attachment to their companion animals at home (PA). Results showed that mean PA scores (47.54 ± 3.6) were significantly higher than mean ZA scores (32.89 ± 2.6; t = –5.16, df = 13, p < 0.001), indicating stronger attachment to the companion animals. PA scores were lower in keepers who thought it inappropriate to have a bond with a zoo animal, compared with those who deemed it appropriate. Thus, HABs do appear to occur in the zoo context, though they are weaker than those developed in the home. This work also shows that a modified LAPS questionnaire is a suitable instrument for further investigation of HABs in zoos.     

Postoccupancy evaluation of staff,visitors, and three species of animals in a zoo setting

Postoccupancy evaluation (POE) was used to assess newly constructed zoo exhibits from the perspective of three user groups: zoo staff, zoo visitors, and the animals. Staff represents a generally understudied user group in zoo-based POEs. We asked staff to rate the animals' space, the visitors' space, and the staff's space at previous and new exhibits. We also compared zoo visitors' ratings of the animals' behavior and environments, overall exhibit impressions, and the time visitors spent viewing previous and new exhibits. Lastly, we compared activity and space use of a Komodo dragon (Varanus komodoensis), two red pandas (Ailurus fulgens), and one rhinoceros (Rhinoceros unicornis) in their previous and new exhibits. Staff rated animal, visitor, and staff areas higher at the new exhibits compared to the previous exhibits. Visitors also rated several factors higher and spent more time at the new exhibits. The most naturalistic exhibit received the most favorable ratings in all categories and animal activity increased visitor stay time. We found that red pandas were less active in their new exhibit, and the Komodo dragon and rhino showed no difference in activity. The red pandas and the Komodo dragon used more available space in their new exhibits; however, we recommend using Electivity index to examine resource preferences for these species, whose enclosure use has been less studied than large mammals. We emphasize the importance of including staff in zoo-based POE, make other recommendations for future POE studies, and discuss various factors that could have influenced our results.     

Visitors' perceptions of zoo‐housed lesser anteater (Tamandua tetradactyla) welfare: Observation plays a larger role than a brief informative talk

There is a growing ethical concern in modern society about animals' quality of life. We hypothesize that zoo visitors' perception of zoo animal welfare, particularly in the case of lesser anteaters, changes positively after listening to scientific information. Visitors observing active lesser anteaters in their enclosures at Córdoba Zoo (Argentina) were asked to respond to a questionnaire about animal welfare. The treatment group (T) answered the questionnaire after listening to a brief informative talk based on local scientific studies on lesser anteaters. The control group (C) answered the questionnaire without hearing the informative talk. Visitors (87.2%) considered biological, sanitary, and sociocultural aspects to be necessary conditions for optimum wild zoo‐housed animal welfare. The majority of visitors considered that natural surroundings provide the highest level of welfare for wild animals. Visitors in the T group ranked the zoo as providing a higher level of animal welfare than those in group C. In reference to management measurements, the T group agreed on the positive effect of the application of environmental enrichment (Likert Medians: C = 4 and T = 5; p = .0443). On the basis of their perception, most visitors in both groups stated that the lesser anteaters at Córdoba Zoo appeared to be in a good state of welfare. We interpret this as meaning that, what these Córdoba zoo visitors personally perceived while observing the lesser anteaters carried greater weight than what they learned from the informative talk, though the talk did slightly affect their opinion.     

Mortality of wild and captive chimpanzees

Mortality of chimpanzees in the wild (Gombe National Park) and in captivity (Taronga Zoo, Sydney and Melbourne Zoo) was compared using standard cohort life table techniques. Overall mortality probabilities up to age 30 were compared using a logrank test. No significant difference in overall mortality was revealed, and the mortality curves did appear to be surprisingly similar, but there were nevertheless some differences in the distribution of mortality. Perinatal mortality was higher in the zoo, while post-perinatal and infant mortality were higher in the wild. Survivorship in the older zoo animals (over age 27) was better than the wild. These differences were attributed to the more sheltered zoo environment, including the availability of veterinary care, which could be expected to improve survival in infants and older adults. The higher perinatal mortality experienced by zoo infants could be reflecting higher levels of inbreeding among the zoo animals.     

A Case for a Naturalistic Perspective: Response to Lawrence and Bekoff

ABSTRACT

We evaluated three forms of primate free-ranging displays at Singapore Zoo, each with varying restrictions on ranging area and freedom for the primates, as well as visitor proximity. The cotton-top tamarin (Saguinus oedipus), the white-faced saki (Pithecia pithecia), and the orangutan (Pongo pygmaeus) displays illustrated differences in primate visibility to visitors, visitor–primate proximity, frequency of visitor–primate interactions, visitor crowd size, and responses. Amongst the three free-ranging displays, the cotton-top tamarins offered the highest visibility, closest proximity between visitors and primates, highest interaction levels, and attracted the largest crowds. However, undesirable interactions occurred most between the cotton-top tamarins and visitors. We found consistently positive visitor perceptions (total n = 464) of all three primate displays in terms of visitor enjoyment (> 95%); naturalistic zoo experience (> 95%); learning experience (> 90%); and the promotion of good welfare (> 90%). Increasingly naturalistic displays of animals in zoos through the free-ranging of animals can have considerable benefits for both zoo visitors as well as animals, and is a display concept that deserves implementation on a wider scale. Design and implementation of such displays should, however, achieve a balance to maximise display value and animal welfare while curtailing the effects of undesirable human–primate interactions through the restriction of visitor–primate proximity.     

Ticks species (Ixodida) in the Summit Municipal Park and adjacent areas,Panama City,Panama

From September 2007 to September 2009, we studied the species of ticks present in the Summit Municipal Park. Ticks were extracted from zoo animals, free-living wild mammals and reptiles trapped, dead mammals on the roads and environment (ground and zoo burrows). A total of 2,649 ticks were collected: 2,167 immature stages (1,345 larvae and 822 nymphs) and 482 adults. Seventeen species were identified: Ornithodoros puertorricensis (Argasidae), Amblyomma auricularium, A. cajennense, A. calcaratum, A. dissimile, A. geayi, A. naponense, A. nodosum, A. oblongoguttatum, A. ovale, A. pecarium, A. sabanerae, A. tapirellum, A. varium, Ixodes luciae, Haemaphysalis juxtakochi and Rhipicephalus sanguineus (Ixodidae), representing 36% of the species reported in Panama. Amblyomma ovale was the species most commonly infesting animals from the zoo.     

Meta‐analytic review of the effects of enrichment on stereotypic behavior in zoo mammals

This meta‐analysis reports the effect enrichment has on the occurrence of stereotypic behavior exhibited by captive zoo mammals. The analysis also identifies which types of enrichment are most effective, which groups of animals benefit the most, and which types of stereotypes are most affected by environmental enrichment. The analysis included 54 studies that yielded 63 effect size statistics. Fifty‐seven of sixty‐three effect sizes went in the predicted direction (90%), with the animals participating in less stereotypic behavior during the enrichment condition than in the baseline condition. The mean effect size (correlation coefficient r) was 0.46. The combined P‐value using both fixed and random effects methods was reveled to be <0.0000001. A file drawer N‐value was calculated to identify the number of unretrieved studies (with a combined effect size of zero) that would be needed to nullify the results of this analysis. The file drawer N‐value was 1,726, suggesting that it is highly unlikely that the significant results reported in this analysis are nullified by studies that remain in file drawers. Based on these results it was concluded that enrichment substantially reduces the frequency of stereotypic behavior exhibited by mammals living in zoo environments. Zoo Biol 0:1–21, 2006. © 2006 Wiley‐Liss, Inc.     

A short review on dermatophytoses of animals in Romania

Dermatophytoses of animals in Romania are reviewed. Ringworm infections have been found in cattle (whereT. verrucosum was the only isolated agent), horses (the causative organisms beingT. verrucosum, T. mentagrophytes andM. equinum), cats (dermatophytes isolated:M. canis andT. quinckeanum), dogs (M. canis andM. gypseum), fowlsT. gallinae). From the laboratory animals: guinea pigs (T. mentagrophytes, M. audouinii, T. rubrum), mice (T. quickeanum andT. mentagrophytes), rats (T. mentagrophytes), rabbits (T. mentagrophytes andM. canis) and hamster)T. mentagrophytes). Among the wild animals, only the chamois had a ringworm infection byM. gypseum, other large or smaller wild animals harboring only saprophytically some poozhilic and geophilic dermatophytes.     

A Systematic Review and Meta-Analysis of the Campylobacter spp. Prevalence and Concentration in Household Pets and Petting Zoo Animals for Use in Exposure Assessments

Animal contact is a potential transmission route for campylobacteriosis, and both domestic household pet and petting zoo exposures have been identified as potential sources of exposure. Research has typically focussed on the prevalence, concentration, and transmission of zoonoses from farm animals to humans, yet there are gaps in our understanding of these factors among animals in contact with the public who don’t live on or visit farms. This study aims to quantify, through a systematic review and meta-analysis, the prevalence and concentration of Campylobacter carriage in household pets and petting zoo animals. Four databases were accessed for the systematic review (PubMed, CAB direct, ProQuest, and Web of Science) for papers published in English from 1992–2012, and studies were included if they examined the animal population of interest, assessed prevalence or concentration with fecal, hair coat, oral, or urine exposure routes (although only articles that examined fecal routes were found), and if the research was based in Canada, USA, Europe, Australia, and New Zealand. Studies were reviewed for qualitative synthesis and meta-analysis by two reviewers, compiled into a database, and relevant studies were used to create a weighted mean prevalence value. There were insufficient data to run a meta-analysis of concentration values, a noted study limitation. The mean prevalence of Campylobacter in petting zoo animals is 6.5% based on 7 studies, and in household pets the mean is 24.7% based on 34 studies. Our estimated concentration values were: 7.65x10³cfu/g for petting zoo animals, and 2.9x10⁵cfu/g for household pets. These results indicate that Campylobacter prevalence and concentration are lower in petting zoo animals compared with household pets and that both of these animal sources have a lower prevalence compared with farm animals that do not come into contact with the public. There is a lack of studies on Campylobacter in petting zoos and/or fair animals in Canada and abroad. Within this literature, knowledge gaps were identified, and include: a lack of concentration data reported in the literature for Campylobacter spp. in animal feces, a distinction between ill and diarrheic pets in the reported studies, noted differences in shedding and concentrations for various subtypes of Campylobacter, and consistent reporting between studies.     

Siamangs (Hylobates syndactylus) and White-Cheeked Gibbons (Hylobates leucogenys) Show Few Behavioral Differences Related to Zoo Attendance

The effect of visitors on behavior and welfare of nonhuman animals in the zoo has been an active research topic during the last few decades. Although research has variously shown negative or positive impacts of zoo visitors on animals in captivity, previous primate research at Disney's Animal Kingdom® suggests the importance of visual barriers in allowing animals to cope with large crowds. Examining this further, this study monitored the behavior of white-cheeked gibbons (Hylobates leucogenys) and siamangs (Hylobates syndactylus) in large, open exhibits. Behavioral data showed rates of social behavior and percentage of time engaged in solitary behavior did not differ between low and high visitor-attendance days. Both gibbons and siamangs spent more time in areas away from the public on high attendance days. Supporting previous findings, results imply visual barriers and ability to retreat from crowds may have provided these animals with choice and minimized potential negative visitor impact. Future research should focus on the relationship between attendance and actual crowds at exhibits; it should utilize multi-institutional methodologies to control for variance and look for individual and demographic differences between individuals.