A number of studies have shown results which are best interpreted as indicating that the presence, and particularly the behaviour, of unfamiliar people (usually zoo visitors) is stressful to zoo animals. For example Chamove et al. (1988) recorded increases in agonistic behaviour and decreases in inactivity and grooming in three different primate species (ringtailed lemur Lemur catta, cotton-topped tamarin Saguinus oedipus and diana monkey Cercopithecus diana) at Edinburgh Zoo when members of the public were present; the changes in behaviour were much less when the visitors were asked to crouch rather than stand in front of the cages. Similarly Mitchell et al. (1991b) found that intra-group aggression doubled when a group of golden-bellied mangabeys was transferred from a cage with low visitor attendance (because of its location within the zoo) to a cage with higher visitor attendance. Most studies have used behavioural measures, but several have used physiological measures. Davis et al. (2005), for example, found that urinary cortisol levels in spider monkeys (Ateles geoffroyii rufiventris) at Chester Zoo correlated positively with the number of visitors to the zoo. Similarly, in black rhinoceros higher mean faecal corticoid levels were found in zoos where the animals were kept in enclosures with a greater degree of public exposure (Carlstead and Brown, 2005). Hosey (2000) reviewed the relevant literature on the responses of zoo animals to human audiences, and used the literature to test three hypotheses, namely, that the behavioural changes were a simple social facilitation effect, that they were the consequence of the audiences being stressful to the animals, and that they were the consequence of the audiences being enriching for the animals. The evidence mostly supported the stressful hypothesis, with some support for the hypothesis that audiences could under some circumstances be enriching, and with no support for the facilitation hypothesis. However, inconsistencies were noted in the behavioural responses recorded in different studies, and it was suggested that these might be the result of differences between species, between housing conditions, and in the way different audiences were perceived. It is also worth pointing out that many of the published studies show an association between the behaviour of the animals and the presence of visitors, but do not necessarily indicate unequivocally the direction of causality. Thus, it is also possible to argue that the animals show elevated activity and agonism for some other reason, and that this greater activity in the cage attracts the audience (Mitchell et al., 1992c). This, for example, was considered by Margulis et al. (2003) to be the best explanation of associations they saw between felid behaviour and visitor presence. The studies reviewed by Hosey (2000) were overwhelmingly primate studies; while this is still the case with the literature, there are now many more studies available, and they show that the situation is even more complex when non-primate studies are available. The available studies are briefly reviewed here by taxonomic group in order to detect whether any trends or differences are apparent between different kinds of animal.
Studies which have involved primates (lemurs and monkeys) and (apes). Looking at the lemurs and monkeys first, there appears to be a reasonable consistency in what the different studies show. In most cases the animals show an increase in locomotion or activity (one redfronted lemur shows a decrease), an increase in agonistic behaviour (but not in the black lion tamarin or the green monkey) and a decrease in grooming and/or affiliative behaviours (but not in the mangabey). This is the suite of behavioural changes that was first suggested by Chamove et al. (1988) to indicate stressful excitement in the animals, and many subsequent studies have followed this interpretation. What about the exceptional cases? The black lion tamarin Leontopithecus chrysopygus, shows no increase in agonistic behaviour, unlike most of the other species. The authors of that report attributed this to a species characteristic, that these were a much ‘‘more relaxed’’ species when visitors were present (Wormell et al., 1996). In Fa’s (1989) study of green monkeys Cercopithecus aethiops sabaeus at Mexico Zoo no increases in agonistic behaviour were seen, but these animals were being fed by the public, so zoo visitors may not have been seen as stressful by the animals. Indeed, visitor-directed behaviours in this group were related to obtaining food. In most of the other studies visitor-directed behaviours have not been scored; the mangabeys Cercocebus galeritus chrysogaster showed elevated intra-group agonistic behaviour and also directed threats at the visitors (Mitchell et al., 1991a, 1992a), whereas the mandrills Mandrillus leucophaeus increased their rates of glancing at the visitors as visitor numbers increased, which again was interpreted as a stressful effect of people on the animals (Chamove et al., 1988).