Visitors' Effects on the Welfare of Animals in the Zoo: A Review

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3 JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 10(2), Copyright 2007, Lawrence Erlbaum Associates, Inc. Visitors Effects on the Welfare of Animals in the Zoo: A Review Gareth Davey Department of Psychology University of Chester, United Kingdom Since the 1970s, research about zoo visitors effects on the welfare of nonhuman animals in captivity has intensified. Numerous studies have shown that characteristics such as visitor presence, density, activity, size, and position are associated with animal behavioral and to a lesser extent physiological changes. Studies usually interpret these changes as negative (undesirable) or positive (enriching), but it remains unclear whether they significantly impinge on animal welfare. To make confident conclusions about visitors effects necessitates more studies using (a) a wider range of animal groupings, (b) measures of stress, (c) visitor animal variables, and (d) other methodological improvements In the meantime, in addition to further research, individual zoos need to emphasize (a) monitoring the stress indicators of their captive animals, (b) observing visitor behavior, and (c) ensuring that staffs are aware of the visitor effect concept. The presence of people at zoo exhibits may be perceived by nonhuman animals in captivity as either a negative influence, a form of enrichment, or simply a changing variable that has no effect (Hediger, 1969; Hornaday, 1930; Hosey, 2000; Kawata, 1971; Morris, 1964; Snyder, 1975). It is therefore imperative that welfare specialists understand the possible influence of zoo visitor behavior on animal well being, either to reduce stressful situations or to utilize opportunities for enrichment. Although, at one extreme, unruly visitor behavior such as teasing, feeding, shouting, and throwing stones are animal welfare concerns (Hediger, 1969), studies since the 1970s have associated the mere presence and typical activities of visitors at exhibits with behavioral and physiological changes in captive animals. Correspondence should be sent to Gareth Davey, Department of Psychology, University of Chester, Parkgate Road, Chester, United Kingdom CH1 4BJ. g.davey@chester.ac.uk

4 170 DAVEY Efforts to understand the relationship between visitors and animal welfare have recently intensified. There seems to be support in the literature for the notion that the presence, density, size, and position of visitors are associated with undesirable and sometimes enriching animal behavioral and physiological changes. To discuss these issues, this review (a) draws together the literature about visitor effects on animals, (b) discusses whether a visitor effect exists, (c) considers the importance of factors such as exhibit design and species type, and (d) discusses the limitations of existing work. Suggestions are provided also for zoos and animal welfare specialists to counteract visitor effects to ensure that animal welfare is not compromised under certain audience conditions. EARLY RESEARCH The earliest studies took place during the 1970s. Thompson (1976) reported increased sexual behavior among chimpanzees in response to higher zoo visitor numbers, and the following year Oswald and Kuyk (1977) observed increases in the frequency of several lorisoid primate behaviors after a primate house was opened to the public. Research continued throughout the 1980s; Glatston, Geilvoet-Soeteman, Hora-Pecek, and van Hooff (1984) noted less social behavior (contact, mounting, and play) of cotton-topped tamarins between groups exposed to visitors and groups away from the public. Maki, Alford, and Bramblett (1987) observed heightened intragroup aggressive behavior by chimpanzees in the laboratory toward conspecifics, scientists, and students at a research facility. Hosey and Druck (1987) advanced the notion of a visitor effect further in the late 1980s in their study of 12 captive primate species. They noticed that visitor presence affected locomotor behavior and spatial dispersion, and more primate behaviors were directed towards active rather than passive visitor groups. Collectively, this handful of studies was important because it revealed that zoo visitors influenced the behavior of captive animals to a greater extent than was previously thought; it also paved the way for further research that now constitutes an increasingly popular topic in zoo animal welfare research. The field has increased in popularity in recent years, and there is now an emerging literature about animals responses to visitor variables such as visitor presence, density, activity, size, and position. The literature is summarized in Table 1 and discussed next. ARE THERE VISITOR EFFECTS ON ANIMAL WELFARE? The summary in Table 1 shows that visitor activities are associated with animal behavioral changes interpreted as ambivalent, negative, or positive in terms of animal

5 171 TABLE 1 The Presence, Density, Activity, Size, and Position of Visitors Have Been Associated With Animal Behavioral and Physiological Changes Species Behavioral Change Visitor Effect Authors Behavioral response to visitor presence Green monkeys (Cercopithecus aethiops sabaeus) Cotton-top tamarins (Saguinus oedipus oedipus) Bare-faced tamerins (Saguinus bicolor bicolor) Chimpanzees (Pan troglodytes) Lion-tailed macaques Macaca silenus) Ungulates (12 species) Lemurs (Lemur catta) Diana monkeys (Cercopithecus diana) Lemurs (Lemur catta) Siamangs (Hylobates syndactylus) Monkeys spent more time around the edges of enclosures, and interacted more with visitors, but no difference in agnostic behavior None Fa (1989) Less social behavior (contact, mounting, and play) when compared Stressful Glatston et al. (1984) to conspecifics housed off exhibit More threats, piloerection, and approaching behavior toward Stressful Wormell et al. (1996) visitors Increased aggressive behaviors toward conspecifics and scientists Stressful Maki et al. (1987) and students at a research facility Presence of visitors was associated with increased levels of pacing, Stressful Mallapur et al. (2005) begging, and self-biting When a zookeeper stood at the front of the exhibit there was Ambivalent Thompson (1989) increased vigilance and approach behavior, lower occurrence of eating and drinking; and increased number of vocalizations Significant increase in aggression; decrease in grooming, Stressful Chamove et al. (1988) inactivity, and affiliative behavior Significant increase in aggression; decrease in grooming, Stressful Chamove et al. (1988) inactivity, and affiliative behavior Significant increase in aggression; decrease in grooming, and Stressful Chamove et al. (1988) inactivity No changes in activity None Nimon & Dalziel (1992) (continued)

6 172 TABLE 1 (Continued) Species Behavioral Change Visitor Effect Authors Golden-bellied mangabeys (Cercocebus galeritus chrysogaster) Responded with threats to visitor presence Ambivalent Mitchell, Herring, Tromborg, et al. (1992); Mitchell, Obradovich, et al. (1991); Mitchell et al. (1990); Mitchell et al. (1987) Cheetahs (Acinonyx jubatus) No significant effect None O Donovan et al. (1993) Penguins (Sphenicus humboldti) Behavioral response to visitor density Gorillas (Gorilla gorilla graueri) Western lowland gorillas (Gorilla gorilla gorilla) Golden-bellied mangabeys (Cercocebus galeritus chrysogaster) Orangutans (Pongo pygmaeus) Chimpanzees (Pan troglodytes) Jaguars (Panthera onca) Significant increase in submerged swimming, and decrease in surface swimming and resting Ambivalent In a group of five animals, four were unaffected and one spend more time near visitors Ambivalent Vrancken et al. (1990) Individuals spent significantly more time nesting when visitor Stressful Wells (2005) density was low, and significantly more intragroup aggression, stereotypies, and auto grooming when visitor density was high Reduced visitor numbers resulted in less visitor-directed Stressful Mitchell, Herring, aggression, decreased within-group aggression, and increased Tromborg, et al. displays toward neighbors (1992) No changes in behavior None Mather (1999) A higher number of wounding episodes in a laboratory colony on weekdays (high levels of human activity) compared to weekends. Visitor density associated with pacing behavior, increased aggression, and nonvisibilty in cage Stressful Lambeth et al. (1997) Stressful Sellinger & Ha (2005)

7 Cotton-top tamarins (Saguinus oedipus oedipus) Mandrills (Mandrillus sphinx) Stump-tailed macaques (Macaca arctoides) Goeldi s monkeys (Callimica goeldii) Orangutans (Ponga pygthaeus) Negative correlation between the duration of affiliative behavior and number of visitors; positive correlation between visitor density and the number of agnostic encounters between mothers and their offspring Increased glancing behavior and threats toward increased visitor density, and a concomitant reduction in affiliative behavior High visitor density positively correlated with increased aggression High visitor density positively correlated with increased aggression, and negatively correlated with grooming Infants held onto adults more, and adults used available paper sacks to cover their heads more during periods of high visitor density Behavioral response to visitor activity, size, and position Talapoin monkeys (Miopithecus Increase in activity and visitor-directed behavior toward active talapoin), brown lemurs (Lemur visitor groups compared to passive ones fulvus), ring-tailed lemurs (Lemur catta), white-fronted capuchins (Cebus albifons), black spider monkeys (Ateles paniscus), lion-tailed macaques (Macaca silenus), de Brazza s monkeys (Cercopithecus neglectus), Sykes monkeys (Cercopithecus mitis), Patas monkeys (Erythrocebus patas), black macaques (Macaca nigra), barbary macaques (Macaca sylvanus), hamadryas baboons (Papio hamadryas) Stressful Glatston et al. (1984) Stressful Chamove et al. (1988) Negative Simpson (2004) Negative Simpson (2004) Stressful Birke (2002) Ambivalent Chamove et al. (1988); Hosey & Druck (1987) 173 (continued)

8 174 TABLE 1 (Continued) Species Behavioral Change Visitor Effect Authors Chimpanzees (Pan troglodytes) Ring-tailed lemurs (Lemur catta), mongoose lemurs (Lemur mongoz), red-ruffed lemurs (Varecia variegate rubra), squirrel monkeys (Saimiri sciureus), francois langurs (Presbytis francoisi francoisi), spot-nosed monkeys (Cercopithecus ascanius schmidti), de Brazza s monkeys (Cercopithecius neglectus), golden-bellied mangabeys (Cercocebus galeritus chrysogaster), gibbons (Hylobates lar), orangutans (Pongo pygmaeus abeli), chimpanzees (Pan troglodytes) Penguins (Sphenicus humboldti) Orangutans (Ponga pygthaeus) Increase in visitor-directed aggressive behaviors, and affiliative behaviors, mother child contact, and locomotion in the presence of active groups; individuals interacted with visitors for food Significantly more behaviors (number of interactions with audience and cage mates, levels of locomotor activity, and spatial dispersion in the cage) directed at active, rather than passive, groups Significantly more time swimming on the surface, and less time swimming submerged, when quieter visitor groups were present Animals looked more at the visitors, and infants approached and held onto adults more, when confronted with noisy groups Ambivalent Ambivalent Cook & Hosey (1995); Perret et al. (1995 Mitchell, Tromborg, et al. (1992) Ambivalent Condon et al. (2003) Ambivalent Birke (2002)

9 VISITORS EFFECTS ON ANIMALS IN THE ZOO 175 welfare. This implies that there is a visitor influence, and animal husbandry staff should be aware of possible relationships between visitors and animal welfare. However, based on existing studies, the behavioral response to visitors and thus the nature of a visitor effect remains difficult to interpret. The first reason is that although visitor and animal behavior are associated, it is difficult to demonstrate causality (Chamove, Hosey, & Schaetzel, 1988; Hosey, 2000; Margulis, Hoyos, & Anderson, 2003; Mitchell, Tromborg, et al., 1992). It has even been argued that rather than an animal response to humans, visitor behavior such as increased visitor density may be caused by animals (Hosey, 2000), and there are some reports in the literature that support this view (Bitgood, Patterson, & Benefield, 1988; Davey, 2006a; Johnston, 1998). Another problem is ambiguity surrounding the measurement and interpretation of stress. The presence of certain types of abnormal animal behaviors is currently used as a stress indicator. Although some behavioral changes may indicate welfare concerns such as an increase in affiliative behaviors (probably good for welfare) and increase in aggressive behaviors or stereotypies (probably bad for welfare), this distinction may be too simple: The use of abnormal behaviors as a poor welfare indicator is complex (Mason, 1991). Further, not all studies that report a stressful influence show changes in agonistic and affiliative behaviors (Mitchell, Herring, et al., 1991; Mitchell, Herring, Tromborg, et al., 1992; Perret, Preuschoft, & Preuschoft, 1995). Some studies include a wide range of behaviors locomotor behavior, mother young interactions, and vigilance that are not always easy to interpret in terms of animal well being. A major weakness of large-scale studies is that visitor presence and typical activities have not been unequivocally demonstrated to actually compromise animal well being. It is not clear if animal behavioral changes are stressful and therefore important. As Hosey (2000) stated: No studies have made predictions about what specific effects a stressful influence should have, but have inferred stress from the observed pattern of behavior (p. 335). This problem stems partly from the fact that studies fail to link observed changes in animals behavioral repertoires to baseline measures or a definitive measure of stress; more accurate measures of well being are needed (Gregory, 2005). The problem of quantifying a visitor effect is hampered further by the literature s focus on reporting behavioral changes, rather than other measures such as physiological changes. Indicators of stress are varied, and simple behavioral measurements may not provide sufficient evidence to draw conclusions. This situation is changing, however, as a few recent studies have revealed relationships between visitor variables and endocrine stress indicators (Davis, Schaffner, & Smith, 2005; Kalthoff, Schmidt, & Sachser, 2001; Wehnelt, Fishlock, Condon, Coleman, & Schaffner, 2004). More work is needed, perhaps using a combination of reliable ethological, physiological, immunological, and neurological methodologies (Gregory, 2005). Other limitations of existing research are discussed later.

10 176 DAVEY CAN THE VISITOR EFFECT BE POSITIVE? On the other side of the coin is the suggestion that zoo visitors enrich the lives of captive animals (Hosey, 2000; Markowitz, Stevens, & Barrow, 1981). According to this view, visitors provide a source of variability and, therefore, environmental enrichment (Hosey, 2000; Markowitz et al., 1981; Moodie & Chamove, 1990; Morris, 1964). Limited research has investigated visitors possible enriching effects, but anecdotal evidence, particularly at zoos and exhibits that allow animal people interactions, or where animals roam freely among visitors, suggests that some animals may seek visitor effects (Hosey, 2000, 2005). Studies are beginning to emerge to support this view. For example, Baker (2004) evaluated the value of a caretaker s additional time (an extra 10 min a day, 5 days a week) spent interacting with chimpanzees at an animal care facility and observed lower levels of abnormal behaviors. In the zoo setting, Cook and Hosey (1995) observed that visitors and chimpanzees engage in a succession of exchanges that come alternatively from visitors and animals. In their study, chimpanzees were motivated to interact with visitors, and visitors provided food for the animals in 25% of the interactions. Although visitors can be considered to be a form of enrichment, this hypothesis has not been tested in the same way that enrichment devices have been assessed such as the incidence of species-specific behavior before and after enrichment. For the time being, it seems that confident conclusions about the direction of visitor effects on animal welfare cannot be made. It is clear, however, that visitors and their behaviors are indeed associated with behavioral and physiological changes in captive animals; further work is needed to evaluate whether visitor effects are significantly enriching or stressful. ENCLOSURE DESIGN AND VISITOR EFFECTS Limited research has explored if enclosure variables are tied to, and interact with, visitor effects. Exhibits that include interactive elements perhaps best exemplify the link. For example, animal parks, petting zoos, and some zoos such as Apenheul in the Netherlands allow animals to range freely among visitors, and these types of enclosure are becoming more popular (Fa, 1989; Hosey, 2000; Kreger & Mench, 1995). As early as 1975, Throp described the advantages of an interactive exhibit that allowed a tug of war of a rope between visitors and a captive gorilla. Yanofsky and Markowitz (1978) described a game that allowed visitors and captive mandrills to interact. The visitor effect may be dampened in naturalistic exhibits in which naturalistic items provide hiding places for animals to escape from visitors. Another factor, as

11 VISITORS EFFECTS ON ANIMALS IN THE ZOO 177 Hosey (2000) commented, is that perhaps larger, more naturalistic cages produce a more naturalistic profile of behavior which is more resistant to disruptions from visitor presence (p. 353). Research has shown that a barrier placed between visitors and animals concealment screens or camouflage nets also reduces the visitor influence (Blaney & Wells, 2004; Mononen, Kasanen, Harri, Sepponem, & Rekila, 2001; Simpson, 2004). For example, Blaney and Wells installed a camouflage net barrier at the viewing area of a gorilla exhibit. They observed a reduction in stereotypical behaviors and lower levels of conspecific-directed aggression, typically induced by large groups of visitors. Environmental enrichment devices may also be important as Wood (1998) found interaction between visitors, enrichment devices, and visitor effects. She noted that the response of chimpanzees (foraging, feeding, and object use) to new and old enrichment devices was reduced when high visitor crowds were present. Research has shown that the location of exhibits may be important (Davey & Henzi, 2004; Mitchell et al., 1990). Mitchell et al. found that a cage near the zoo entrance received significantly more visitors than those further away, whereas Davey and Henzi observed unequal exhibit popularity in a primate house due to exhibit location. This has important implications because unbalanced or large numbers of visitors at specific enclosures could present a stressful influence: Visitor animal interactions are positively correlated with visitor density (Fa, 1989). For example, a study by Mitchell, Herring, et al. (1991) showed that the mangabeys (Cercocebus galeritus chrysogaster) when they were moved to cages with higher visitor density increased both their aggressive displays toward visitors and their aggression within groups. ARE SOME SPECIES OR INDIVIDUALS MORE PRONE TO A NEGATIVE VISITOR INFLUENCE? Most studies have focused only on captive primates and a limited number of species; therefore, it is difficult to draw confident conclusions about differences in visitor responses across animal groups. However, Table 1 shows that the visitor effect is not the same for all species. One reason may be body size. It has been suggested that small species such as arboreal primates may be particularly prone because visitors may be perceived as potential predators and are likely to respond with avoidance and defensive behavior; in contrast, larger animals may be nonresponsive to visitor disturbance or may display offensive threats (Chamove et al., 1988; Hosey, 2000; Margulis et al., 2003). Because smaller animals such as cotton-top tamarins (Saquinus oedipus) seem to respond negatively, the studies listed in Table 1 provide support for this suggestion; however, larger animals such as orangutans, gorillas, and felids are less affected (Mather, 1999; Margulis et al., 2003; O Donovan, Hindle, McKeown, & O Donovan,

12 178 DAVEY 1993; Vrancken, Van Elsacker, & Verheyen, 1990). Other possible explanations why different species respond to visitors differently include species variation in social organization, typical responses to environmental events, and species-typical habituation to visitors (Hosey, 2005). There is also some evidence that primates can identify and respond differently to different categories of visitors. An intriguing finding, for example, was that golden-bellied mangabeys responded differently to keepers (familiar humans), observers (less familiar humans), and visitors (unfamiliar humans) and directed more frequent aggressive facial displays toward human visitors of the same sex (Mitchell, Herring, & Obradovich, 1992; Mitchell, Herring, Tromborg, et al., 1992; Mitchell, Obradovich, Herring, Dowd, & Tromborg, 1991). It may be that individual differences gender, size, and personality also interact with the visitor effect, although research on this topic is lacking (Davey, 2005b; Hosey, 2000; Mitchell, Herring, Tromborg, et al., 1992; Thompson, 1989). Other factors that also require further elucidation include the influence of social groups and hierarchy, whether animals are captive born, duration of captivity, time-of-day, and seasonal differences. HOW CAN THE QUALITY OF RESEARCH BE IMPROVED? If results are to provide deeper insights and be of practical benefit for advancing animal welfare, there is a need for improvement in how research is conducted. Improvements suggested in this review include the use of more precise measures of animal stress, inclusion of a wider range of animal groupings, and acknowledgment of previously overlooked variables such as animals individual differences and social hierarchy and groups. There is a disproportionate amount of research across different visitor variables and animal groupings. Most research has focused on the effect of visitor presence and visitor density, whereas little work has explored visitors activities, size, and proximity (Table 1). Further, most studies have focused on captive primates. Much more research is needed using a wide range of visitor variables and animal groupings. There are also methodological weaknesses of existing work. A major problem is the large number of uncontrolled variables (enclosure designs and management procedures) not accounted for in research designs. This difficulty is usually overcome in other biological and psychological research through the control and manipulation of independent variables; however, the real world nature of zoo research means that fewer independent variables can be controlled. For example, Wells s (2005) study of gorilla behavior during winter weekdays (low visitor numbers) and summer weekends (high visitor numbers) failed to account for factors

13 VISITORS EFFECTS ON ANIMALS IN THE ZOO 179 such as seasonal differences in behavior (Ross, Lonsdorf, & Stoinski, 2007), as well as the fact that different demographic groups of visitors (and therefore visitor behavior) visit at different times of the year (Broad, 1996). Studies tend to use vague and insufficient descriptions of visitor variables. An example is the division of visitor groups into active and passive in order to understand the influence of visitor activities (Hosey & Druck, 1987; Mitchell, Tromborg, et al., 1992). Hosey and Druck defined active groups as those in which at least one person attempted to interact with the animal (p. 23). Yet, because many visitor behaviors could be included, this behavioral measure and its definition are insufficiently detailed. A more meaningful division could be to define different types of activity pointing, tapping on glass, or waving and different intensities of each behavior. Another example is the use of zoo attendance figures as a measure of visitor numbers at a specific exhibit (Davis et al., 2005; Mallapur, Sinha, & Waran, 2005); studies could be improved by using absolute measures of visitor numbers at specific exhibits. Further, whereas existing studies have grouped visitor density into large and small groups, a better approach may be statistical correlations between visitor numbers and changes in animal behavior (Chamove et al., 1988; Davey, 2006c; Hosey, 1997; Jones & Wehnelt, 2003). Low sample size is a recurring issue in zoo research. Many studies (Sellinger & Ha, 2005; Vrancken et al., 1990; Wells, 2005) have used low animal sample sizes, which means that any observed responses to visitors may be specific to individuals; results may not necessarily generalize to other situations. This problem may be reduced when researchers pool data about animals from several enclosures or zoos (Mallapur et al., 2005); however, because this method increases the number of uncontrolled differences that exist between enclosures and zoos, it is also problematic. It is also important to note that most studies, using univariate statistical methods, have investigated the influence of one or two factors on visitor behaviors. This poses serious consequences on their inferential value; a larger number of factors and more advanced statistical methods are needed (Johnston, 1998; Kuhar, 2006). Last, research is limited by its independence from other areas of visitor research (Davey, 2006b; Davey & Henzi, 2004; Davey, Henzi, & Higgins, 2005). Visitor research is conducted in zoos, museums, botanical gardens, science centers, and across many disciplines such as sociology, education, and psychology. However, studies about zoo visitor effects have been conducted in isolation, and findings are reported in different journals and conferences (Davey, 2006b). Interaction between research areas will be beneficial for animal welfare researchers and will likely lead to the provision of more effective zoo programs and exhibits (Davey, 2006b; Davey et al., 2005). As an example, Davey and Henzi found that a visitor behavioral pattern previously reported from museums also existed in a zoo primate house and resulted in marked variations in visitor density and therefore possible visitor effects between exhibits.

14 180 DAVEY FURTHER RESEARCH AND MINIMIZING VISITOR EFFECTS The studies reviewed previously have important implications for the practical management of animal welfare. If visitors and their activities are associated with animal behavioral and physiological changes, then the next step is to consider ways of reducing or eliminating possible negative effects. Extra emphasis should be placed on monitoring the stress indicators of captive animals. Although further work is needed with specific exhibits and species to determine if visitor effects actually exist, zoo staff particularly keepers and exhibit and enrichment designers can take several measures to minimize possible negative effects. First, it is important that staff understand the concept and literature pertaining to the topic and conduct their own research. This can be done at both established exhibits and during the planning stage of exhibit design (Davey, 2006b). Although specific solutions should be implemented following research, some general suggestions will now be offered. Counteractions to reduce visitor presence at exhibits include one-way viewing glass, a dry moat barrier, and camouflage nets. The counteractions also include changing the size of viewing windows, altering the height of walkways, and considering the location from which visitors can view animals. The effects of visitor density can be reduced by understanding changes in visitor density, understanding how visitors travel within zoos, balancing visitor numbers by placing popular exhibits such as those housing popular animals or exhibit designs in less-visited areas, or housing species that are typically less responsive to visitors where visitation rates or behavior are higher (Davey & Henzi, 2004; Margulis et al., 2003). Conversely, species that are sensitive to visitors could be placed toward less visited areas, such as the final stages of defined paths in a zoo. CONCLUSIONS Numerous studies have shown that visitor variables such as visitor presence, density, activity, size, and position are associated with animal behavioral and to a lesser extent physiological changes. Although the reported changes are inferred, often as a possible stressful or enriching experience, more research is needed before confident conclusions about visitors influences on animal welfare can be drawn. Future studies should include a wider range of animal groupings, measures of stress, and visitor animal variables. In the meantime, zoo staff should be aware of the concept and literature about visitor effects and conduct their own research at specific zoos and exhibits to monitor stress indicators.

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