The Impact of Visitors on Non-Primate Species in Zoos: A Quantitative Review.

Visitors are a prominent feature in the lives of zoo animals, and their presence can cause a range of impacts on zoo animals (typically classed as positive, negative or neutral impacts), commonly referred to as the 'visitor effect'. This paper quantitatively collates the literature on the visitor effect in non-primate species, investigates the types of measures used to assess impacts of visitors on animals and considers whether impacts vary across non-primate species in zoos. In total, there were 105 papers which had investigated the impact of zoo visitors on 252 non-primate species/species groups. There has been a steady increase in visitor effect research in zoos since 2012 and this body of work incorporates species from avian (28% study species), reptilian (9%), amphibian (2%), fish (4%) and invertebrate taxa (1%). However, there is still a bias towards mammalian species (56%). The response to visitors varied across taxa. Amphibians responded negatively to visitors more frequently than would be expected by chance (p < 0.05), birds responded neutrally more frequently than would be expected by chance (p < 0.05) and fish responded neutrally and 'unknown' more frequently than would be expected by chance (p < 0.05). This review highlighted a number of animal-based metrics which have been used to assess the impacts of visitors on animals, with measures used varying across taxa. Moving forwards, it is recommended that moving forwards researchers incorporate a suite of measures, incorporating those which are meaningful in terms of being representative of individual animal experiences and animal welfare, collected in a manner which should capture those metrics accurately.

Furred and feathered friends: How attached are zookeepers to the animals in their care?

Keeper-animal relationships (KARs) appear to be important in zoos, since they can enhance the well-being of both the animals and the keepers, can make animal husbandry easier, but conversely might risk inappropriate habituation of animals and possible risks to the safety of keepers. It is, therefore, important to know more about the variables involved in relationship formation. Here we use a modified version of the Lexington Attachment to Pets Scale (LAPS) to measure the strength of KARs between keepers and animals in their care, both in the zoo and in the home. LAPS questionnaires were completed by 187 keepers in 19 different collections across three countries. LAPS scores for attachment to zoo animals (ZA) were significantly lower than for pet animals (PA). There was no significant difference in ZA scores between different taxa, but there were significant taxon differences between PA scores. There were significant differences in both ZA and PA scores between different collections. Female respondents scored more highly than males for both ZA and PA. Multiple regression revealed that location, gender, and time spent with animals were significant predictors for ZA, while only gender and taxon were significant predictors for PA. It was concluded that PA scores were comparable with those for the general public, and reflected strong attachment of keepers to their pets, while ZA scores, although also reflecting attachment, were influenced by differences in institutional culture.

Zoo-housed mammals do not avoid giving birth on weekends.

There is evidence that zoo visitor presence can influence the behaviour and, in some cases, adrenal response of zoo animals, and can sometimes compromise animal welfare. In some laboratory studies, significantly more primate births have been reported on weekends, when fewer people are working there, compared with weekdays when staffing levels are at their highest. Here, we investigate whether there is evidence of a "weekend effect" on births in zoo animals as a result of visitor numbers. Unlike laboratories, zoos are typically busier with visitors on weekends than on weekdays, although staffing levels remain fairly consistent across days of the week. If zoo animal parturition is sensitive to human presence, then fewer births would be expected on weekends compared with weekdays. We tested this using birth data and visitor numbers on the entrance gate from zoo records across 16 species representing artiodactyls, perissodactyls, carnivores and primates at four British zoos, to see whether there is an association between mean daily birth rates and average visitor numbers. We predict that, if there is a visitor effect, daily births should be lower on weekends than weekdays and should correlate with mean daily visitor numbers. Results showed that births for all 16 species were randomly distributed through the week, and there was no significant decline in births on weekends. We conclude that the "weekend effect", if such a thing exists, does not appear to be a feature of zoo births, suggesting that elevated weekend visitor numbers are not sufficiently stressful to trigger delayed parturition.

The Need for a Convergence of Agricultural/Laboratory and Zoo-based Approaches to Animal Welfare.

Advances in animal welfare science have led to a high number of studies published for farm, laboratory and zoo animals, with a huge breadth of innovative topic areas and methodologies. This paper investigates the different approaches used to undertake welfare research in farm, laboratory and zoo animals due to the variety of constraints that each group brings. We also set recommendations to how groups can support each other in moving forwards to reduce animal suffering and promote a life worth living, a goal that all parties aim to achieve. We propose that researchers develop more collaborations across species, in particular to focus on the applied component of animal welfare and utilizing positive welfare indicators; facilitate knowledge transfer and share good practice worldwide; and accept small n based studies that can still be scientifically robust and provide individual-based steps into advances in our knowledge. Ultimately, we need to be progressing animal welfare science to a point beyond legislative needs, and ensure that "high animal welfare" becomes an additional mission statement for all animal-based industries.

Is wounding aggression in zoo-housed chimpanzees and ring-tailed lemurs related to zoo visitor numbers?

Chimpanzees in laboratory colonies experience more wounds on weekdays than on weekends, which has been attributed to the increased number of people present during the week; thus, the presence of more people was interpreted as stressful. If this were also true for primates in zoos, where high human presence is a regular feature, this would clearly be of concern. Here we examine wounding rates in two primate species (chimpanzees Pan troglodytes and ring-tailed lemurs Lemur catta) at three different zoos, to determine whether they correlate with mean number of visitors to the zoo. Wounding data were obtained from a zoo electronic record keeping system (ZIMS™). The pattern of wounds did not correlate with mean gate numbers for those days for either species in any group. We conclude that there is no evidence that high visitor numbers result in increased woundings in these two species when housed in zoos. Zoo Biol. 35:205-209, 2016. © 2016 Wiley Periodicals, Inc.

Are we ignoring neutral and negative human-animal relationships in zoos?

Human-animal interactions (HAI), which may lead to human-animal relationships (HAR), may be positive, neutral, or negative in nature. Zoo studies show that visitors may be stressful, may have no effect, or may be enriching. There is also evidence that good HARs set up between animals and their keepers can have positive effects on animal welfare. However, we need to know more about negative HARs, and as a first step we attempt to do this here by considering cases where animals attack people in the zoo. Due to the sensitivity and rarity of these events data appear sparse and unsystematically collected. Here, information available in the public domain about the circumstances of these attacks has been collated to test hypotheses about negative HAIs derived from a model of zoo HARs. The limited data presented here broadly support the zoo HAR model, and suggest that attacks usually happen in unusual circumstances, where there may be a failure by the animal to recognise the HAR, or where the relationship, if there is one, does not hold; and give some support to the prediction that exposure to many keepers may impair the development of a positive HAR. This study may provide useful information for the zoo community to proactively collect systematic standardised records, which will enable a fuller understanding of zoo HARs, upon which appropriate measures might be adopted to build better zoo HARs, which are likely to positively impact zoo animal welfare, and reduce these rare incidences further.

Hediger revisited: how do zoo animals see us?

Contact with people, both familiar (e.g., caretakers) and unfamiliar (e.g., members of the public), is a significant part of the lives of nonhuman animals in zoos. The available empirical evidence shows that in many cases this contact represents a source of stress to the animals, although there is sufficient overall ambiguity in these studies to suggest that the effect of people on the animals is much more complex than this. A possible way to try to understand human-animal relationships in the zoo is to ask how the animals might perceive the humans with whom they have contact, and here this question is explored further, using a framework first published by Hediger as a starting point. Hediger suggested that zoo animals might perceive people as an enemy, as part of the inanimate environment, or as a member of the same species. He supported these categories with anecdotal evidence, which was all that was available at the time, but more empirical evidence is available now, so it is appropriate to revisit these categories. The evidence suggests that animals discriminate both conspecific and heterospecific others, rather than just viewing familiar people as members of their own species, and that additional categories (stimulating part of the environment and friendship) may be warranted. These categories are then placed in a general model that suggests how relationships of different qualities, and hence different perceptions of each other, might develop between animals and the people they are in contact with in zoos.

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.

Can zoo records help answer behavioral research questions? The case of the left-handed lemurs (Lemur catta).

Most zoos keep comprehensive records, which potentially form a database for use in answering some research questions, such as in veterinary and population management research. They have not, however, been widely used to answer questions about animal behavior and welfare. Here we try to assess the usefulness to behavioral research of two sorts of zoo records (ARKS, the Animal Records Keeping System, and student dissertations held on file) to test the hypothesis that ring-tailed lemurs with a left limb preference experience more negative social lives. We found that, as predicted, lemurs with a left limb preference (LH) received more aggression and were involved in less grooming than nonleft-preferent lemurs (NLH), though the differences were not statistically significant. Contrary to prediction, LH lemurs had fewer reported woundings than NLH lemurs, but again the difference was not statistically significant. We found that the ARKS reports did not contain sufficient quantified and systematic behavioral data for our purposes, although otherwise they provided an excellent context for interpreting results. The student dissertations were also of limited use, primarily because of the small time frame in which they were carried out. Because of these shortcomings we were unable to distinguish whether our inability to find significant effects was due to biological (perhaps hand preference had no consequences for the lemurs) or data reasons. We suggest that closer liaison between zoo research staff, zoo record keepers and academic supervisors could help to improve the usefulness of zoo records for behavioral research.