The Visitor Effect on Zoo Animals: Implications and Opportunities for Zoo Animal Welfare
Abstract
:Simple Summary
Abstract
1. Introduction
1.1. Zoo Animal Welfare
1.2. The Human Environment in Captive Animal Settings
1.3. Zoo Visitors
2. Assessment of the Visitor Effect
2.1. Metrics Studied
2.2. Study Design Approaches
3. Direction of the Effect
3.1. Negative Impacts
3.2. Neutral Effects
3.3. Positive Effects
4. Discussion of Possible Explanatory Factors
4.1. Species Evolutionary Traits
4.2. Individual Traits
4.3. Environmental Features
5. Future Directions
Funding
Acknowledgments
Conflicts of Interest
Appendix A
Species | Visitor Variable | Animal Measure | Results | Reference |
---|---|---|---|---|
Primates | ||||
Baboon | Presence vs. absence | Behaviour | When transferred to a new enclosure that was on display to the public, the male baboon increased throwing behaviour, which included throwing objects or faeces at visitors or staff. | [89] |
Black-capped capuchin | Visual contact * | Behaviour and GCs | Reducing visual contact with visitors resulted in a reduction in group aggression, GC concentration, abnormal behaviour and avoidance of viewing area. | [52] |
Chimpanzee | Number | Behaviour | High visitor numbers were associated with lower frequencies of foraging, grooming and play. | [96] |
Interaction sequences | Behaviour | Both chimpanzees and visitors regularly initiated interaction. Chimpanzees interacted with humans primarily to obtain food. | [107] | |
Number | Behaviour | There was no effect of crowd size on chimpanzees’ use of the areas of their exhibit closest to zoo visitors. In addition, they were observed in this area at a rate equal to or greater than expected by random movements at all three levels of crowd size analyzed. | [154] | |
Number | Behaviour (birth timing) | An analysis of the timing of 231 live chimpanzee births in accredited North American zoos found no weekend (high visitor numbers) or weekday (low visitor numbers) effect on number of births. | [155] | |
Colombian spider monkey | Number | Urinary cortisol | An increase in visitor numbers was associated with an increase in urinary cortisol concentration. | [13] |
Cotton top tamarin | On display vs. off display | Behaviour | The animals on display to the public exhibited less social behaviour than those not displayed to the public. | [91] |
Diana monkey | Number | Behaviour | Higher visitor numbers were associated with less time spent grooming and sleeping/resting and more time spent playing and feeding/chewing. | [109] |
Diana Monkey, ringtail lemur, cotton-top tamarin | Presence vs. absence | Behaviour | When visitors were present, aggression levels increased, and time spent engaged in grooming and other affiliative behaviours decreased. | [75] |
Height of visitors * | Behaviour | When visitors were asked to crouch, grooming behaviour increased and agonistic behaviour decreased. | ||
Golden-bellied mangabey | Number * | Behaviour | Animals moved to cages that were exposed to more visitors increased their aggressive displays towards visitors and increased within-group aggression. Animals displayed more threatening behaviour towards visitors than they did towards keepers or other primates. | [73] |
Lion-tailed macaque | Presence vs. absence | Behaviour | Conducted at eight sites: On days when visitors were present, the frequencies of abnormal behavior, including self-biting, begging and bouncing, were significantly higher, and social behaviour and visibility were significantly lower. | [156] |
Mandrill | Number | Behaviour | As visitor numbers increased, mandrills showed a reduction in time spent engaged in affiliative behaviour and increased time spent watching and threatening visitors. | [75] |
Orangutan | Number | Behaviour | During periods of high visitor density, adults used paper sacks to cover their heads more and infants held onto adults more. | [77] |
Noise * | Behaviour | When confronted with noisy groups, animals spent more time looking at the visitors, and infants approached and held onto adults more. | ||
Visual contact * | Behaviour | Orangutans showed a preference to position themselves facing towards the open window of the visitor viewing area. | [16] | |
Number | Behaviour | A high visitor number increased time spent looking at visitors and begging. | [141] | |
Behaviour | Behaviour | Visitors with food and visitors who were looking or taking photographs increased the time orangutans spent looking at visitors, begging and moving. | ||
Proximity | Behaviour | Closer proximity between visitors and orangutans decreased the time orangutans spent playing/engaging in social behaviour and increased the time spent looking at visitors and begging. | ||
Pileated gibbon | Number | Behaviour | A higher visitor number was associated with increased levels of self-biting. | [94] |
Ring-tailed and Mayotte lemurs, black spider monkey, white-fronted capuchin, Patas monkey, De Brazza’s monkey, Sykes monkey, talapoin, Barbary, lion-tailed and Sulawesi macaques and Hamadryas baboon | Number and behaviour | Behaviour | Animals showed more locomotion and directed more behavior towards visitors when confronted with small active and large active audiences rather than passive audiences. | [157] |
Ring-tailed, mongoose and red-ruffed lemurs, squirrel monkey, Francois langur, spot-nosed monkey, De Brazza’s monkey, golden-bellied mangabey, gibbon, orangutan and chimpanzee | Number and behaviour | Behaviour | Animals directed more behaviour towards visitors when confronted with active audiences than passive audiences. | [79] |
Ring-tailed lemur | Number and behaviour | Behaviour | As the number of visitors increased, time spent in locomotion and on the ground increased. However, visitor behaviour did not impact lemur behaviour. | [158] |
Number | Behaviour | Visitor numbers were associated with a decrease in foraging, resting and sunbathing and an increase in locomotion and alertness. However, these effects were reduced when weather was accounted for in the statistical model. | [72] | |
Siamang | Number | Behaviour | There was no difference detected in behaviour according to visitor number. However, siamangs appeared to respond to some human behaviours as they would to hostile behaviours from their own species. | [106] |
Siamang, white-cheeked gibbon | Number | Behaviour | On days of higher visitor numbers, both siamangs and gibbons spent more time in areas away from the public and were less visible. There were no differences in rate of aggressive or affiliative interactions under different visitor numbers. | [85] |
Sulawesi macaque | Number and noise | Behaviour | Conducted at five sites: As visitor numbers and noise increased, locomotion, vigilance and foraging increased and social huddling and resting decreased. | [159] |
Western lowland gorilla | Visual contact * | Behaviour | Reducing visual contact with visitors resulted in lower levels of conspecific-directed aggression and stereotypies. | [12] |
Number and Noise | Behaviour and GC | High numbers of visitors and higher noise levels increased staring and charging at visitors and decreased food-related behaviour. No effects on GC concentration. | [61] | |
Visual contact * | Behaviour and GC | When privacy screens were in place, staring and charging at visitors decreased. No effects on GC concentration. | ||
Number | Behaviour | Conducted at two sites: One site found no effect of visitors and the other site found higher visitor numbers were associated with increase in duration of self-scratching and visual monitoring when no enrichment was provided. | [54] | |
Number | Behaviour | Conducted on two groups: When large crowds were present, both groups were less visible. One group (bachelor group) also showed more aggressive behaviour with large crowds. | [92] | |
Number | Behaviour | Conducted on four groups: Higher visitor numbers resulted in higher levels of stereotypies in two groups and males also showed increased aggression. | [131] | |
Number | Behaviour (birth timing) | An analysis of the timing of 336 live gorilla births and 48 stillbirths at 53 accredited North American zoos from 1985–2014. Results showed no weekend (high visitor numbers) or weekday (low visitor numbers) effect on number of births or stillbirths. | [160] | |
Number | Behaviour | There was no effect of crowd size on gorilla use of the areas of their exhibit closest to zoo visitors. In addition, they were observed in this area at a rate equal to or greater than expected by random movements at all three levels of crowd size analyzed. | [154] | |
Number | Behaviour | High visitor numbers were associated with significantly more intragroup aggression, stereotypies and autogrooming, whereas a low visitor number was associated with a greater proportion of time spent resting. | [93] | |
White handed gibbon | Number and Noise | Behaviour | Higher numbers of visitors and higher noise levels resulted in increases in ‘look at public’ behaviour in all four gibbons. Higher noise levels also increased self-scratching behaviour in two individuals. One male showed an increase in aggressive ‘open mouth’ and ‘teeth display’ in response to the increased group size and noise level. | [55] |
Carnivora | ||||
Brown bear | Presence vs. absence | Behaviour | The presence of visitors was associated with greater levels of stereotypies, locomotion, vigilance and increased use of the back part of the enclosure. | [95] |
Cheetah | Number and noise | Behaviour | No difference in cheetah behaviour was detected in response to visitor number. | [101] |
Clouded leopard | Presence vs. absence | GCs | Higher GC concentrations in animals housed on display versus off display. | [40] |
Eurasian lynx, ocelot, bobcat, jaguar, Asiatic lion | Presence vs. absence | Behaviour | Conducted at two sites: when visitors were present (zoo open), ocelots, lynx, bobcat and lions showed a decrease in activity and an increase in time spent further away from visitor areas, but the jaguar showed the opposite response. | [161] |
Fennec fox | Number | Behaviour | Higher number of visitors was correlated with increased frequency of stereotypic running. | [35] |
Giant panda | Presence vs. absence | Behaviour | Presence of visitors was associated with greater levels of exploration, feeding and time spent not visible. Pandas also showed an increase in use of the back part of the enclosure when visitors were present. | [95] |
Harbour seal | Number | Behaviour | Under increasing visitor numbers, more seals were submerged under water. | [162] |
Indian leopard | Presence vs. absence | Behaviour | Conducted at four sites: leopards rested significantly more when visitors were present. | [163] |
Jaguar | Number and behaviour | Behaviour | When the visitor numbers and intensity of behaviour were lowest, jaguars spent more time non-visible. The female showed an increase in pacing behaviour at the intermediate level of intensity of visitor behaviour recorded. | [84] |
Presence vs. absence | Salivary cortisol | Conducted at two sites: At one site, ‘open to the public’ days were associated with increased levels of salivary cortisol compared to ‘no visitor’ days. There was no significant relationship detected at the other site. | [164] | |
Lion, Amur leopard, Amur tiger, Snow leopard, clouded leopard, fishing cat | Presence vs. absence | Behaviour | No effect of visitor presence or absence on felid activity patterns. | [15] |
Puma | Number and noise | Behaviour | With higher numbers of visitors and noise levels, pumas increased time spent inactive and engaged in visitor-directed vigilance. | [98] |
Meerkats | Visitor behaviour (noise) * | Behaviour | Conducted at three sites: No change in meerkat behaviour in response to a reduction in intensity of visitor behavior. | [14] |
Mexican wolf | Number | Behaviour and GCs | Conducted at three sites: higher numbers of visitors were associated with higher GC concentration and less time spent lying and eating. | [97] |
Ungulates | ||||
Asian elephant, Indian rhino | Presence vs. absence | Salivary cortisol | Salivary cortisol concentrations were found to be significantly higher during the opening period (where animals had their first direct visual contact with visitors that year) compared to during pre- and post-opening periods. | [165] |
Black rhino | Number | GCs | Higher mean GC concentrations were found at zoos where rhinos were maintained in enclosures that were exposed to the public around a greater portion of the perimeter. | [70] |
Indian blackbuck | Number | Behaviour and GCs | Higher numbers of visitors were associated with higher GC concentration, increased levels of aggression and less time resting. | [100] |
Indian gaur | Presence vs. absence | Behaviour | When visitors were present, animals showed higher levels of intragroup aggression and moving behavior and less resting behavior. | [90] |
Sika deer | Number | Behaviour | High visitor numbers were associated with deer spending less time foraging and more time being watchful, resting and ‘non-visible’. | [87] |
Soemmerring’s gazelle | Number | Behaviour | Conducted on three groups: animals in enclosures that were most accessible to visitors, had higher agonistic reactions than animals housed in enclosures with less exposure to visitors. | [88] |
Marsupials | ||||
Koala | Proximity | Behaviour | Greater numbers of visitors within a 5 m radius of koalas resulted in more visitor-vigilant behavior. | [78] |
Noise level * | Behaviour | When ‘loud’ crowd noise playbacks were played to koalas, they were significantly more likely to be disturbed than ‘quiet’ crowd noise playbacks. | ||
Quokka | Presence vs. absence * | Behaviour | Fewer quokkas were visible when the enclosure was open to visitors. | [76] |
Red kangaroo and Kangaroo Island kangaroo | Visitor number | Behaviour and GCs | Conducted at two sites: when visitor numbers increased, both species of kangaroos increased time spent vigilant towards visitors and Kangaroo Island kangaroos increased time spent engaged in locomotion and decreased time spent resting. No effect of visitor numbers on faecal GC concentration or distance from path. | [86] |
Rodents | ||||
Black-tailed prairie dog | Number | Behaviour | Under higher visitor numbers, prairie dogs moved closer to visitors. | [108] |
Penguins | ||||
African penguin | Number | Behaviour | Presence of visitors in a pool adjacent to the penguin pool reduced the time penguins spent in their pool. | [99] |
Gentoo penguin | Number | Behaviour | Higher numbers of visitors were associated with greater behavioural diversity and increased pool use by penguins. However, neither visitor behaviour nor enrichment appeared to affect behavioural diversity. | [110] |
Little penguin | Presence vs. absence * | Behaviour | Presence of visitors increased levels of aggression, huddling and behaviours indicative of avoidance such as hiding and increased distance from viewing area. | [53] |
Other birds | ||||
Corella | Number | Behaviour | When there were fewer visitors present, Claude the corella spent more time engaging in ‘attention-seeking’ behaviours to initiate interaction with visitors. | [106] |
Greater rhea | Presence vs. absence | Behaviour | In the presence of visitors, rheas increased walking alert behaviour. | [166] |
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Sherwen, S.L.; Hemsworth, P.H. The Visitor Effect on Zoo Animals: Implications and Opportunities for Zoo Animal Welfare. Animals 2019, 9, 366. https://doi.org/10.3390/ani9060366
Sherwen SL, Hemsworth PH. The Visitor Effect on Zoo Animals: Implications and Opportunities for Zoo Animal Welfare. Animals. 2019; 9(6):366. https://doi.org/10.3390/ani9060366
Chicago/Turabian StyleSherwen, Sally L., and Paul H. Hemsworth. 2019. "The Visitor Effect on Zoo Animals: Implications and Opportunities for Zoo Animal Welfare" Animals 9, no. 6: 366. https://doi.org/10.3390/ani9060366