Human–animal relationships (HAR) in the zoo – Familiar humans

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The literature on caretaker–animal relationships in laboratory-housed exotic animals is sparse, and despite some early discussion as to whether positive relationships between humans and laboratory animals could become so positive that they could be regarded as bonds (Davis and Balfour, 1992), the extensive application to exotic animals of the HAR concept used in farm animal research has not really been seen so far. There is in fact no particular reason why we cannot conceive of HARs developing between exotic animals and their keepers, not only in laboratories but also in zoos. An important difference, however, between the zoo environment and the laboratory and farm is the daily presence of large numbers of zoo visitors, and it would be surprising if the quality of animal interactions with zoo visitors were not influenced, and in turn had an influence upon, the relationship that the animals have with their keepers. Thus, in applying the HAR concept to the zoo setting, we need to consider human–animal interactions involving familiar (keepers, other zoo personnel, zoo researchers) and also unfamiliar (zoo visitors) humans.

Familiar humans
Heini Hediger, who wrote extensively about the different aspects of the zoo environment, and who can probably be regarded as the founder of modern zoo biology, suggested that, of the various ways in which humans might be perceived by zoo animals, keepers were likely to be seen as conspecifics. This could lead to two possible risks: ‘‘the animal sees the keeper as a rival of the same sex and this leads to aggressive behaviour, or it sees in him a potential mate and this may present a danger to the keeper owing to importunate attempts to mate with him’’ (Hediger, 1970, p.83). These views, based on many years’ experience, were nevertheless made within the ethological framework of the time, and now, forty years on, we can conceive of relationships between animal and keeper that do not have to be based on dominance or imprinting. The important point, however, is that zoo animals probably see the keepers in a different way from the way they see the public (the latter as an enemy, in Hediger’s system). For our purposes here, we could re-frame this view in terms of the likelihood that animals in zoos will develop a HAR with their keepers, but may have a different, and probably generalised, relationship with the visiting public. Few systematic studies have been undertaken on animal–keeper interactions, so evidence for the HAR in zoo animals is sparse. A study by Thompson (1989) of 12 different ungulate species showed that the animals displayed more vigilance towards keepers when the keepers were in rather than in front of the enclosure, and they showed more vigilance towards keepers when the public were not present. When the zoo was closed to the public, females, but not males, of large species showed more vigilance towards keepers than small-bodied species. Although superficially this resembles an anti-predator response (i.e. the animals viewed public and keepers as potential predators), Thompson felt that this interpretation was not fully consistent with the data, and that curiosity and monitoring to maintain social cohesion was a better explanation of the changes in behaviour. Responses of golden-bellied mangabeys (Cercocebus galeritus chrysogaster) to both familiar and unfamiliar people at Sacramento Zoo were studied by Mitchell et al. (1991a). These animals threaten people, other monkeys and even inanimate objects. Mitchell et al. (1991a) found that most threats were directed at human visitors, with keepers and observers (i.e. the experimenters) receiving far less threats. It is possible that the animals behaved in this way simply because the visitors and the keepers were behaving towards them in different ways. Nevertheless these authors concluded that zoo visitors were treated like interlopers, keepers like familiar conspecifics, and observers like familiar neighbours. Other primates also behave differently to different categories of humans. Colobus monkeys (Colobus guereza) at Paignton Zoo, for example, show different frequencies of interaction with keepers, zoo staff (anyone wearing a zoo uniform but not involved in day-to-day care of those animals) and zoo visitors (Melfi and Thomas, 2005). Interestingly, interactions with all three categories reduced significantly (interactions with zoo visitors stopped altogether) after positive reinforcement training of the animals to facilitate oral examination. Studies like these indicate that animals as different as primates and ungulates behave differently towards familiar and unfamiliar humans, but do not necessarily provide evidence that HARs have been set up. Some support for the hypothesis that zoo animals establish HARs with their keepers comes from studies on small felids. Mellen (1991), investigating the factors that were associated with reproductive success in small cats, found that, amongst other things, the quality of keeper interactions with the cats was a significant predictor of the cats’ reproductive success. In particular, a husbandry style characterised by keepers talking to the cats, and interacting with them, was more likely to be associated with the cats having offspring than a style which did not include such interaction. As a consequence, Mellen (1991) recommended that positive human–animal relationships were desirable for successful reproduction, and that this should start with a socialization process involving, for example, stroking and playing with kittens, the aim being to produce cats with a reduced fear of humans but an enriched environment to facilitate normal behavioural development. In clouded leopards (Neofelis nebulosa) faecal corticoid levels were associated negatively with the amount of time primary caretakers spent with the animals, but positively with the number of keepers (Wielebnowski et al., 2002). This was interpreted as indicating that a higher number of keepers probably meant that a predictable, high quality relationship between keeper and cat could not be set up, because individual keepers spent less time with the animals. Finally, in white rhinoceros (Ceratotherium simum), animals which keepers had rated highly in terms of ‘‘friendliness to keeper’’ had significantly lower mean levels of faecal corticoids (Carlstead and Brown, 2005). Although not directly giving evidence of a HAR in these animals, this is nevertheless consistent with the hypothesis that a positive relationship with the caretaker has beneficial effects on the animal’s welfare.