Chapter 10 Primates and Pachyderms: A Primate Model of Zoo Elephant Welfare Terry L. Maple1,2 Mollie A. Bloomsmith2,3 and Allison L. Martin1,2,3 School of Psychology1 and Center for Conservation and Behavior2 Georgia Institute of Technology and Yerkes National Primate Research Center of Emory University3 The public and professional debate about the efficacy of exhibiting elephants in captivity has reached a fevered pitch. In a headline from the June 11, 2006 issue of Time Magazine, the author opined: “It may be that some animals just can’t be kept humanely in captivity” (Lemonick 2006). Notably, five major zoos in Chicago, Detroit, Philadelphia, New York and San Francisco have decided to stop exhibiting elephants, and officials of the Bronx Zoo have elected not to replace their animals at the end of their lifespan. Clearly, for those zoos intent on continuing an elephant program, it has become much more difficult and expensive to provide for elephants, as there is little agreement on the nature and scope of an elephant’s needs in captivity. As the elephant controversy plays out in the media, the debate is reminiscent of the challenge to properly exhibit and meet the needs of nonhuman primates in the zoo. Monkeys and apes benefited from the constructive dialogue among primate experts and zoo professionals. American zoos have justified the exhibition of elephants in much the same way that apes in captivity have been justified; the animals serve a noble purpose in educating the public about wildlife, and zoo professionals have committed to organized in situ conservation programs managed through the Species Survival Plan (SSP) of the AZA. It may be instructive to revisit how the psychological well-being of apes and monkeys became a priority. Significant advances in primate exhibition and management took many years to gain traction within the zoo profession, and exhibit innovations were not implemented easily or cheaply. Improvements and innovations in the management of nonhuman primates were based on decades of laboratory and zoo management experience and research, and the application of sound husbandry principles derived from the observations of dedicated field biologists. Of course, there is no single-species primate model that can be applied to elephants or any other animal housed in the zoo. Our model of elephant management, therefore, is comprised of recommended best practices and relevant data-based findings from a diversity of taxa, with great apes receiving special emphasis. In this chapter, we will explore the approach that has been taken to improve the welfare of captive nonhuman primates, and argue that a similar approach may be helpful in advancing the welfare of captive elephants.

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Hard architecture In his 1974 book Tight Spaces, environmental psychologist Robert Sommer defined and delineated the concept of “hard architecture” and its effects on animals confined in the zoo: “The hard zoo consisting of concrete boxes, steel bars, and fixed routine of feeding, watering, and washing by outside maintenance personnel, distorts the behavior of the animals...If living creatures cannot be left in their original habitat, the least that can be done is to place them in natural and responsive surroundings—natural so that their character is not warped, and responsive so that their individuality and creativity are firmly respected” (p. 69). More than 30 years since Sommer established his position, we are still trying to find a way to preserve the character, individuality and creativity of elephants in our zoos. Professor Sommer’s construct of “hard architecture” is a historical benchmark that divides progressive naturalistic exhibitory from the practices that Sommer scorned. Characterized by zoo architects (e.g., Coe 1985) as “landscape immersion,” Sommer used the term “soft architecture” to describe comfortable, flexible, moveable surroundings that function as the virtual antithesis of a rigid, hard and restricted environment. Sommer’s (1974) comparison of zoos and prisons, similar in form and function, accurately portrayed the prevailing zoo exhibit trends as he observed them in the 1960s and 1970s (Figure 1). Eventually, the hard zoo model was replaced by superior, naturalistic zoo designs and landscape immersion architecture (cf. Jones, Coe & Paulson 1976) influenced, in part, by the pertinent research of comparative psychologists (e.g., Yerkes 1925, 1943; Kummer and Kurt 1965; Harlow 1971; Erwin, Maple & Mitchell 1979; Maple 1980; Maple & Hoff 1982; Beck & Power 1988) and field primatologists (e.g., MacKinnon 1974; Goodall 1986; Harcourt 1987; Altmann & Muruthi

Figure 1. Salient example of hard architecture in an American zoo, New Orleans, c. 1976. 130

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1988). This dramatic change in exhibit philosophy and design profoundly affected zoo animal welfare, and nonhuman primates prospered from the innovations that followed. Soft exhibits, large enough to encourage the formation of appropriate primate social groupings, enabled normal reproduction, parenting, social development and rehabilitation (Ogden, Finlay & Maple 1990), and reduced the incidence of abnormal and stereotyped behavior (Clark, Juno & Maple 1982). When exhibits are furnished properly, providing opportunities to manipulate and utilize objects and vertical space, monkeys and apes adjust with species-typical behavior unseen in the hard zoo environment (McKenzie, Chamove & Felstner 1986; Maple & Perkins 1996). Socially deprived zoo gorillas translocated from sterile, restricted (hard) environments into naturalistic exhibits have recovered sufficiently to become breeders (Winslow, Ogden & Maple 1992). However, as ubiquitous as landscape immersion has become, there are still too many examples of hard architecture in world zoos, and many exhibits do not function naturally, despite the appearance of naturalism. While primate exhibits have often been a zoo’s first priority for enrichment and innovation, many other species still reside in substandard facilities. Indeed, elephants, the largest terrestrial mega-herbivores, arguably have benefited least from the revolution in naturalistic zoo design. In hard zoo facilities, elephants are subjected to a life on concrete, surrounded by gunite and steel barriers, harsh chemicals to wash down the containment building and a routinized schedule of management. In fact, Dimeo-Ediger (2001) found that 91 percent of the zoos she surveyed confined elephants on concrete surfaces indoors. Surprisingly, a majority of the surveyed institutions (67 percent) ranked a change in flooring as a low priority. As this survey was conducted in 1997, it may indicate that substrate had not yet received sufficient attention as a management issue. The fact that the Association of Zoos and Aquarium’s (AZA) elephant guidelines for this period (1997) do not mention substrate is another indication that the issue was not yet a blip on the zoo radar screen. Zoo elephants typically spend more than 12 hours per day on hard substrates in night houses, some of them restrained from movement by chains (Bashaw, Burks, Daniel & Maple 1999). It is not surprising that serious foot problems have been documented in 50 percent of captive elephants at some point in their lifetime. Experts (e.g., Csuti, Sargent & Bechert 2001) have reached a consensus, stating that “lack of exercise, long hours standing on hard substrates and contamination resulting from standing in their own excreta are major contributors to elephant foot problems” (p. vii). In the same volume, the esteemed veterinarian Murray Fowler (2001) advised that more exercise would be beneficial for all elephants, facilitated by a written exercise program, and that each “elephant facility should minimize the amount of time elephants spend on hard, unyielding surfaces” (p. 147). AZA’s standards for elephant management and care now require a written daily exercise program for each elephant. Some critics of elephant facilities in the zoo have advocated sanctuaries as healthy, naturalistic alternatives, but the application of principles derived from sanctuary management practices can also serve to enrich and improve a hard, zoo enclosure. An intriguing paper by Buckley (2001) suggests that standard zoo exhibits can be softened. By monitoring elephants at the Hohenwald Elephant Sanctuary in Tennessee, she determined that foot health was facilitated by contact and the curative action of grassland, wetland and forest substrate. She recommended that key features of the natural habitat be “imitated” and natural substrates added to the zoo environment: “For indoor facilities, floors can be remodeled with a more suitable surface. Diets can be modified to include live vegetation and daily supplements of fresh-cut browse...Attending to the natural and basic needs of the elephant will help to ensure healthy feet as well as overall mental and physical wellbeing” (p. 55). 131

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Similarly, visionary zoologist Jeremy Mallinson (1980; 1982) long ago lamented that zoo gorillas typically spent one-third of their lives confined to hard night structures. He argued that such facilities should be softened by the provision of flexible hammocks, deep straw litter and other natural materials. After Mallinson argued this point, it became politically correct to speak to the heretofore subjective design issue of “comfort.” In the preparation of their book, Gorilla Behavior, Maple and Hoff (1982) interviewed experienced field biologists who similarly acknowledged that structural “flexibility” was an essential component of the natural habitat and a variable worthy of attention when designing zoo facilities. Zoos that exhibit apes now routinely provide them with soft, manipulable materials such as deep straw litter, wood wool, tree cuttings or shredded paper. Soft architecture for apes and pachyderms Naturalistic architecture for gorillas took a giant leap forward with the construction of Seattle’s Woodland Park gorilla facility in 1977 (Jones, Coe & Paulson 1976; Hancocks 1979; Coe 1985). The Seattle design firm of Jones and Jones made their reputation on the realism of this innovative exhibit. The landscape topography was varied with mounds and berms and included trees suitable for climbing. Gorillas used these features of the environment even more than the planners expected. To achieve landscape immersion objectives, the design team referenced authentic African field settings to create and implement habitat innovations. Gorilla expert Dian Fossey visited Seattle to provide an expert field perspective for the designers. The contrast between the former, hard cage and the newly planted gorilla forest was striking indeed. Woodland Park’s habitat approach to primate enclosure design was widely imitated but rarely replicated by zoos throughout the world. However, the genie was out of the box, and zoos could no longer justify tiny, hard enclosures for nonhuman primates. Although the gorilla exhibit in Seattle was a simulation of an African rainforest environment, the opportunity to exhibit a group of gorillas proved to be the more influential innovation. After the success of Woodland Park, other zoos aspired to exhibit gorillas in naturalistic social groups, abandoning the misguided tradition of exhibiting isolated singletons and pairs. A decade after Woodland Park, Zoo Atlanta’s Ford African Rainforest exhibited for the first time a population of gorillas in distinct groups occupying five contiguous habitats. The evolving exhibit concept was described (Maple & Finlay 1986) prior to the exhibit’s debut in 1988. Atlanta’s innovations benefited from a home-grown great ape research program at the zoo that was initiated in 1970 by collaborating scientist Dr. Richard K. Davenport of the Yerkes Primate Research Center and Georgia Tech. The continuous participation of Yerkes scientists and veterinarians for two decades provided a foundation for innovation and empirical management practices at the zoo. The Atlanta design team, working with the Philadelphia-based design firm CLR, entered the field in 1986 and 1987 to study the habitat and social life of gorillas and orangutans, returning with new ideas and insight that aided our programming effort. Breeding within the Ford African Rain Forest exhibit commenced immediately after the formation of social groups, with 25 motherreared offspring over three generations produced to date (1988-2008), a strong indication that the appropriate features of the physical and social environment have worked together to facilitate gorilla reproduction (Figure 2). The orangutan exhibit in Atlanta featured a 56-foot-high climbing structure providing a standard of verticality never before accomplished in a zoo. Further innovation has continued in the design of great ape enclosures throughout the nation. Both the San Diego Zoo and Bronx Zoo opened sophisticated gorilla exhibits in the 1990’s, introducing the public to high-tech immersion stimuli including simulated rainforest sounds and artifacts. All recent gorilla exhibits have followed the trend of appropriate social groups, including a number of all-male groups formed because females have not been available. The Fort Wayne (Indiana) Children’s Zoo 132

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Figure 2. After forming social groups in a large, naturalistic enclosure, gorillas at Zoo Atlanta bore the first two offspring in the zoo’s long history. (Photo by Joe Sebo)

orangutans live in a space that is flooded with water. This has promoted their natural arboreal behavior as the residents spend 99 percent of their time moving through trees and climbing structures, closely resembling the locomotion and vertical propensities of wild orangutans (Hebert & Bard 2000). Chimp Haven, a chimpanzee sanctuary in Louisiana, has recently constructed outdoor habitats as large as five acres, with natural trees and vegetation that encourage climbing and daily nest building. One drawback of living vegetation is its vulnerability to the harvesting propensities of apes and other creatures. Elephants are even more destructive, so institutions that plant their exhibits heavily must be prepared to replace them on a regular basis. To adequately prepare for the impact of elephants on their enclosures, zoo planners should consult field experts as they have done with nonhuman primate exhibit design. To this end, elephant expert Cynthia Moss consulted in 1985 with Zoo Atlanta exhibit designers to provide direction on the most important exhibit elements for African elephants. The designers planned and built a 40,000-gallon, naturalistic deep water hole for the elephants, but Moss advised that mud-wallows would be more compelling. The water hole was a great success with zoo visitors when the elephants could be induced to enter it, but the elephants exhibited pure and unrestrained joy whenever the weather provided opportunities to wallow in mud. Moss clearly demonstrated to Zoo Atlanta’s managers that nature is the superior model for zoo designers. Psychopathology Robert Sommer (1974) observed that nonhuman primates in zoos exhibited signs of psychopathology including sexual aberrations, hyper-aggression and a kind of blandness resembling clinical depression. These and other abnormal behaviors are produced by isolation and social 133

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deprivation. Harlow (1971) and his colleagues and students so thoroughly studied these phenomena in the laboratory that we have a detailed understanding of the variables that control them. Indeed, captive monkeys and apes raised by their mothers in species-appropriate social groups and large, complex facilities, are likely to exhibit normal, species-typical behavior (Beck & Power 1988; Bloomsmith, Pazol & Alford 1994). Given nearly ideal circumstances and a tested assortment of best management practices, we know how to foster the development of normal social behavior in monkeys and apes. Because we are able to reconstruct or simulate the essential features of natural habitats and have studied in depth the social life of primates in the field, laboratory and zoo, today we are doing a better job of exhibiting them. Elephants too are prone to abnormal behaviors induced by isolation and restriction. The most common stereotypy emitted by captive elephants is “swaying in place,” and it is more prevalent when elephants are restrained by chains (Friend & Parker 1999; Gruber, Friend, Gardner, Packard et al. 2000). Although it may serve some functions (e.g., coping, or promoting blood circulation inhibited by prolonged inactivity), stereotyped behavior is generally considered evidence of inadequate welfare (Mason 1991). Traditionally, elephants have been chained (or tethered) at night to prevent them from fighting when unsupervised by keepers, and when they are subjected to medical examinations or procedures. Although enlightened zoos have abandoned chaining at night (e.g., Brockett, Stoinski, Black, Markowitz & Maple 1999), temporary chaining for veterinary examination is still common. As elephants are typically active for 18-20 hours in the wild, captive elephants surely benefit from a greater opportunity to move about at all hours. The innovation of “night safaris” for zoo guests is providing an unexpected bonus for zoo animals such as giraffes, rhinoceroses, lions, leopards, hippopotamuses and elephants that prefer to be active at night. Some zoos are leaving elephants in their exhibits overnight to promote continuous locomotion and social interaction. Night access to soft and more natural surfaces outdoors has the added benefit of keeping the elephants off the night quarters hardscape for prolonged periods, and may improve foot health or reduce infection from exposure to pools of urine and feces. Of course, by substituting soft surfaces for hardscapes throughout the building and the exhibit, elephants would benefit day and night (e.g., Meller, Croney & Shepherdson 2007). Cognitive capacity The established continuity between apes and humankind was a compelling reason to enrich and improve environments for nonhuman primates in zoos. The advanced cognitive capacity of monkeys and apes was demonstrated by test after test in the latter half of the 20th century (e.g., Cheney & Seyfarth 1990; Washburn & Rumbaugh 1991; Call & Tomasello 1999). Great ape subjects performed so well in sign and other non-verbal language systems that scientists have compared their abilities to young human subjects. Some writers who raised their subjects in human surroundings regarded them as essentially “enculturated” (e.g., Miles 1994; Miles, Mitchell & Harper 1996) with a vast and largely unexplored potential to learn. However, the idea that an animal must reach a certain criterion of “intelligence” to qualify for an improved quality of life cannot be justified. Highly active species such as anteaters, bush dogs, capybaras, secretary birds and zebras, most of which have not been tested by psychologists, also need room to roam and things to do. As Burghardt, Ward and Rosscoe (1996) have demonstrated, even sessile reptiles can benefit from enrichment. The challenge of animal welfare is to identify the stimuli that trigger natural behavior in all of the taxa that live in the zoo. It is best to be egalitarian when it comes to saving or serving wildlife; big or small, bright or not so bright, beautiful or plain, each and every taxon deserves equal comfort and opportunity to express its species-appropriate character. 134

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In the wild, there is no disputing elephants’ ability to communicate within a complex network of other elephants. Nor can we deny the knowledge they acquire in a lifetime of living in a challenging, changing environment. In the wild, elephants are highly adaptable, and this may bode well for their ability to adapt to changing circumstances in the zoo, including the challenge of translocation for breeding purposes, fewer social partners and limited space. But only a few controlled studies of elephant cognition have been published (e.g., Rensch 1957; Nissani, Hoefler-Nissani, Lay & Htun 2005; Plotnik, deWaal & Reiss 2006). Any scientifically-founded conclusions about the cognitive abilities of elephants will have to await the conduct and replication of additional controlled studies with a systematic approach to measuring these capacities. On the other hand, by observation, anecdote and inference, credible field biologists have claimed a near-human cognitive capacity for elephants (Douglas-Hamilton & Douglas-Hamilton 1975; Moss 1988; Shoshani & Eisenberg 1992; Vauclair 1996; Poole 1998). In our opinion, the observational and experimental data produced so far do not yet elevate elephants to intellectual equivalence with primates. Until a definitive study is published, we are comforted by the fact that a high degree of intelligence, as measured by some standard test or evaluation, is not a requirement for advancing the psychological well-being of captive elephants. Quantity and quality of space If we established a minimum standard of at least 1.5 acres per elephant, a facility with three adult females (the minimum suggested group size) would require 4.5 acres to meet this benchmark. There are not many elephant exhibits in American zoos that currently meet this arbitrary standard. Disney’s Animal Kingdom has three elephant exhibit spaces between 1.5 and 3.5 acres each (J. Lehnhardt, pers. comm. November 8, 2006). North Carolina Zoo has reopened its elephant facility. Expansion of the outdoor habitat from 3.5 to 7 acres has allowed the zoo to increase its herd from three to seven elephants. The facility includes a $2.5 million elephant barn with heated floors, an in-roof sprinkler system for showering the animals and closed circuit television for remote monitoring (AZA Connect, June 2008. p 47). The planned breeding center for elephants developed by the Pittsburgh Zoo will be built on 724 acres on a former Pennsylvania hunting preserve. Clearly, American zoos are starting to think bigger about elephant exhibits. We believe bigger is better, but no one really knows how big is best, so it is likely that exhibits will just get bigger and bigger until the public is satisfied that elephants are “living large” enough in zoos (Kane, Forthman & Hancocks, Appendix I). What does nonhuman primate research reveal about this issue? In their studies of captive apes, Wilson (1982) and later Perkins (1992) found that quality of space was more important than mere quantity of space. The zoos they studied in Europe and America provided moveable objects and opportunities to manipulate and carry balls, boxes, furniture and toys of many different shapes and kinds. The objects also influenced social relationships as they stimulated competition, conflict, play and locomotion. Studies of cage-housed monkeys have found that changes in cage size (up to doubling the space) has little influence on indicators of well-being such as abnormal behavior, environmental manipulation, activity cycle, cortisol levels and food consumption (Goosen 1988; Bayne & McCully 1989; Line, Morgan, Markowitz & Strong 1990; Line, Markowitz, Morgan & Strong 1991; Crockett, Bowers, Sackett & Bowden 1993; Jorgensen, Kinsey & Novak 1997; Crockett, Shimoji & Bowden 2000). Instead, it is not the space itself, but what is within the space that really counts. Monkeys’ use of particular locations in a cage depends upon function (e.g., perching, food provision, view) (Crockett, Yamashiro, DeMers & Emerson 1996). In a review of cage furniture in the zoo, Maple and Perkins (1996) examined all the various types of furniture 135

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that influence enclosure quality for a variety of mammals. A rich environment is important for elephants as they have unique abilities to manipulate objects with their flexible trunks and their sensitive feet. In the field they use their feet to kick clumps of dirt while they grasp and tear grasses and plants with their trunks. The heavy tusks of African elephants are used to stabilize tree trunks as they lean forward to push them over and expose the edible root system. They also excavate with their trunks, thus exposing water sources, locating salt and gaining access to soft, mineral-rich dirt. Maki and Bloomsmith (1989) provided dead trees to enrich chimpanzee enclosures in a Texas chimpanzee facility, and this technique might work well with zoo elephants (see Kinzley 2006). Group size and social organization Gorillas did not begin to breed successfully until zoos abandoned dyads and established groups of three or more animals as the standard unit of social organization. In Howlett’s Park, UK, the largest single groups of lowland gorillas are comprised of more than 20 animals, resembling the size of large mountain gorilla families in Central Africa. However, gorillas also breed in smaller groups with one to three females, and this is the norm for most American zoos (one male: 2.7 female gorillas: Stoinski, pers. comm. November 11, 2006). The trend toward larger, natural groupings of lowland gorillas has been deferred, if not circumvented, by the zeal to build new gorilla exhibits, drawing animals away from zoos capable of exhibiting larger social units. Larger groups, including groups with multiple adult males, provide species-appropriate age and gender balance, enable a richer social milieu and a more accurate representation of gorilla life in the wild, and provide opportunities to study groups in captivity similar in composition to wild social units. However, due to the excellent breeding record in AZA institutions, the association’s Species Survival Plan (SSP) committee for gorillas has elected to widely disperse gorillas to improving facilities with smaller social groups. In this case, the trend toward improved, naturalistic exhibitory trumps group size. In the wild, elephant social organization varies for males and females. Female elephants live in matriarchal herds ranging from eight to 12 animals (Buss & Smith 1966; McKay 1973; Moss 1982; Sukumar 1994), although there is some information indicating Asian elephant groups are somewhat smaller. In zoos, female elephants are typically housed with other females, and males are kept apart, usually alone (Schulte 2000). Captive groups are much smaller than groups living in the wild, with a mean size of 3.4 animals (Bashaw, Burks, Daniel & Maple 1999) in captivity. AZA’s revised standards for elephants (2001) require that no female elephant be kept alone and recommends that groups be comprised of at least three elephants. In terms of exposure to peers, the range of ages represented in a group is greatly reduced in captivity as compared to wild norms. In Africa, newborns live in a rich and supportive social milieu comprised of an array of potential social partners, playmates and allo-parents. Only the larger zoos such as San Diego Wild Animal Park, the North Carolina Zoo and the safari parks have succeeded in establishing anything close to natural social groups. Reflecting the trend, the last elephant “herd” at Lion Country Safari in Florida was dispersed in 2007. Disney’s Animal Kingdom has reached a group size of 12 animals, producing four offspring so far. However, Disney, like the majority of its zoo peers, are breeding through artificial insemination so their commitment to naturalistic exhibitry has limits. Activity and health While we condone the larger, more complex and socially stimulating exhibits built for primates in the 20th century, it appears that these facilities have not met every requirement to promote good health. Many Western lowland gorillas in the zoo die of heart disease in their late 20s and 136

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early 30s, but a thorough analysis of the etiology of this trend is not yet available. Given the established lifespan for lowland gorillas in captivity (54 yrs), the fact that chimpanzees and orangutans have lived into their late 50s, and the belief that mountain gorillas can live more than 60 years in the wild (Fossey 1983), it is evident that many lowland gorillas in American zoos have suffered a premature demise. Given the documented role of these factors in human mortality, it is reasonable to conclude that obesity or a lack of activity (or both) have contributed to this outcome. If gorillas are not using their available space to exercise—and we have evidence they do not (e.g., Ogden & Maple 1990)—it would be prudent to induce locomotion through environmental incentives and training. Naturalistic zoo exhibits are no guarantee that elephants will not themselves become “barn potatoes.” As an additional precaution, we should engineer living space so it elicits normal behavior in real time. We need to design and operate environments that require the animals living in them to search for food, to work to obtain food in species-appropriate ways, to move long distances each day and to engage in a full range of locomotion (see Kinzley 2006). For elephants, locomotion does not just mean walking, but perhaps also swimming, climbing, reaching, lifting, digging and running. Similarly, we assume that elephants must locomote regularly and often to promote proper circulation. Soft substrates alone may not be sufficient to promote healthy extremities. Confining an elephant at night and restriction by chaining prohibits an active lifestyle. Therefore, zoos should consider providing more access to exhibit yards at night. Except in extraordinary and temporary circumstances, we believe chaining should be abolished (Brockett, Stoinski, Black, Markowitz et al. 1999). There must be sufficient space to promote activities such as those listed above, so exhibit size and complexity are both factors in facilitating locomotion. Autonomy and opportunity Caretakers can become enablers of lazy elephants who are over-controlled or over-fed. Put another way, elephants do not benefit from micro-management; they need time and opportunity to behave like elephants and freely interact with peers. Since many elephants have been subjected to traditional circus training methods at some point in their past and many have been subjected to the restrictions of a “coercive carnival culture,” they must be retrained if they enter a more humane system of positive control. The only transitions we have studied are from free contact (FC) to protected contact (PC) training. Wilson, Stone, Bloomsmith and Maple (in prep.) recently evaluated the effects of such a transition at Zoo Atlanta and found that three cow elephants were only slightly less compliant under PC than they were under FC control. It may be that resistance to signals from trainers is the beginning of a greater sense of autonomy. Although compliance is necessary if animals are to benefit from training and from contact for medical purposes, an emerging degree of confidence and volition may produce psychologically healthier individuals. However, if keepers enter the enclosure of more confident, more autonomous and less compliant elephants, they do so at considerable risk. Protected contact likely influences elephant autonomy so the elephant becomes more of a free agent, and the caretaker (for safety reasons) must distance him/herself from the elephant. We regard this typology of “wildness” as a good thing with other zoo animals, but our history of dominating elephants keeps us from fully accepting the elephant’s reversion to wildness. So far, though, we have no evidence that weaning elephants from aversive control has made them more aggressive or more dangerous. Aversive control For elephants, traditional management methods associated with hard zoo architecture have 137

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typically included chaining and aversive methods of control and discipline. Like prisons, hard zoos tend to invoke “hard time” in an inflexible, controlling system of excessive management. Training techniques honed in the Asian logging and the traditional circus industries require hands-on, aversive control methods. Accordingly, elephants are dominated by coercive handlers who utilize the hooked “ankus” to poke and prod them into compliance. Proponents of aversive control have argued the ankus is not painful but is merely a prompt to control or motivate the subject. Critics of the tool disagree, arguing that the ankus can be, and sometimes is, forcefully applied so as to penetrate the skin and cause injury to underlying tissue and bone. A careful reading of the operant psychology literature is helpful in assessing training techniques used with elephants and brings to light other reasons why punitive systems are problematic. Experts in behavior modification have long preached against the use of aversive control methods. Iconic behaviorist B. F. Skinner disdained punishment. Early in his distinguished career (1953) he acknowledged the short-term utility of a severe punisher to interrupt behavior, observing “in the long run...punishment does not actually eliminate behavior from a repertoire, and its temporary achievement is obtained at tremendous cost in reducing the over-all efficiency and happiness of the group” (p. 190). There is no question that punishment, when delivered correctly, will result in at least a shortterm reduction in the occurrence of a problem behavior. However, many factors make aversive control an inefficient method for long-term behavioral control. First, punishment can lead to a cycle of re-emergence of the behavior targeted for elimination. Elephants are often trained to “hold” or stand still on command. A trainer using aversive control might accomplish this by applying the ankus whenever the elephant moves. It is easy to imagine that the elephant might move less and stand still more in this situation. Two forces are at work here. First, moving is punished by the use of the painful ankus. This punishment will decrease the time the elephant spends moving around. Second, standing still is reinforced because that behavior results in removal of the ankus (and associated pain). This type of reinforcement (where the reward is the removal of an aversive stimulus) is called negative reinforcement. As with any form of reinforcement, it will result in an increase in the occurrence of the reinforced behavior (in this case, the elephant standing still). However, if the elephant continues not to move, the ankus will no longer be presented. In this case, it is the actual removal of the ankus that is rewarding the elephant for standing still, and logically, if the ankus is not presented, it cannot be removed. If the ankus is not removed, standing still is no longer rewarded. When a behavior is no longer rewarded (whether with positive reinforcement or with negative reinforcement), the behavior will decrease. So, the behavior of standing still will decrease and the elephant will once again begin moving during the “hold” command. The result, therefore, is not the total elimination of the problem behavior but is instead a cycle of re-emergence that must repeatedly be punished (Skinner 1953). Another difficulty with the use of aversive control is that, in order to suppress a behavior effectively, punishment must follow nearly every occurrence of the behavior (Azrin, Holz & Hake 1963; Appel 1968; Farley 1980). However, this is rarely achieved in practice (Skinner 1953). Another problem has to do with punishment magnitude. Generally only high-intensity punishment will result in a sufficient reduction of the punished behavior (Azrin 1960; Church 1969; Williams, Kirkpatrick-Sanchez & Iwata 1993). To further complicate matters, animals have been shown to adapt to the delivery of punishment (Capaldi, Sheffer, Viveiros, Davidson et al. 1985), and as a result, punishment of constantly-increasing magnitude must be applied to suppress a behavior. Even if a punishment is very intense, it can be ineffective if it has only been used intermittently in the past (Shemer & Feldon 1984; Halevy, Feldon & Weiner 1987) or if the punishment is first 138

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delivered at a low intensity and the intensity is increased gradually (Miller 1960; Cohen 1968). The ineffectiveness of low-intensity punishers often drives the person delivering the punishment to increase the intensity of the punishment until the behavior is successfully eliminated. Described by animal trainers (e.g., Laule & Whittaker 2001) and researchers of human child abuse (e.g., Kadushin & Martin 1981; Straus 2000), this escalation of punishment intensity can lead to abuse. For example, many documented instances of child abuse begin as an attempt to correct the child; however, if the child does not comply, fails to react to the punishment or is aggressive to the parent, the parent subsequently increases the intensity of the punisher, sometimes to abusive levels (Kadushin & Martin 1981; Marion 1982; Straus 2000). Similar circumstances have been noted in animal training, and these effects may be magnified when dealing with large, powerful animals where high magnitude punishers including BB guns or cattle prods have been used (Laule & Whittaker 2001). In addition to being ineffective and possibly leading to abuse, the use of punishment can also produce undesirable side effects. Perhaps the most-studied side effect of punishment is aggression. In the laboratory, the delivery of physical punishment has been shown to elicit aggression in a variety of animal species (Ulrich & Azrin 1962; Azrin, Hutchinson & Hake 1963; Azrin, Hutchinson & Sallery 1964; Azrin, Ulrich, Hutchinson & Norman 1964; Ulrich & Craine 1964; Ulrich, Wolff & Azrin 1964; Azrin, Hutchinson & McLaughlin 1965; Ulrich & Azrin 1962; Azrin, Hake & Hutchinson 1965). This aggression can be directed toward the individual delivering the punishment or toward another animal that is nearby when the punishment is delivered (Ulrich & Azrin 1962; Azrin, Hutchinson & Sallery 1964; Azrin & Holz 1966). Punishment-induced aggression toward a therapist has also been documented in children being treated in human clinical settings (e.g., Mayhew & Harris 1978). Applied to the elephant situation, the delivery of a painful stimulus (e.g., ankus) could cause the elephant to charge and strike a trainer or keeper to stop the delivery of punishment, or the animal may aggress (redirect) against nearby animals. Given the possible deadly effects of elephant aggression, a sensible approach would be to avoid the possibility of punishmentinduced aggression entirely. Other side effects associated with punishment can include an erosion of the relationship between the person delivering punishment and the person or animal being punished, and an increase in other undesirable behaviors. When punished, an animal may associate the punisher with the person delivering it or the context in which the punisher is being delivered rather than with the problem behavior itself (Pryor 1995). For example, dogs trained with shock collars displayed more stress-related behaviors around their owners than those trained with other methods, even when observed outside of the training context (Schilder & van der Borg 2003). The authors of this study concluded that the dogs associated their owners with the administration of the shock. This association can lead the animal to avoid the person delivering the shock or other aversive stimulus (Appel 1961; Azrin & Holz 1966; Boren & Colman 1970), which would be an undesirable outcome for animals being cared for in a zoo. In addition, when one behavior is suppressed through punishment but no appropriate, alternate behavior is trained, other behaviors may increase (e.g., Risley 1968). For example, the elephant may stop moving its feet during a “hold” command but may increase swaying back and forth or swinging its trunk. Thus, instead of one behavior that must be punished, the elephant trainer may end up with countless behaviors to be suppressed. Another potentially worrisome finding in the literature is that punishment corresponds with increases in self-stimulation, such as stereotyped behavior, in humans (e.g., Epstein, Doke, Sajwaj, Sorrell et al. 1974; Doke & Epstein 1975; Rollings, Baumeister & Baumeister 1977; Wells, Forehand, Hickey & Green 1977). This is a major concern given the desire to reduce stereotypies 139

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in captive elephants. Given the inefficiencies, side effects and possible dangers associated with the use of aversive control, it is not surprising that so many zoos have adopted protected contact methods, a more efficient behavioral management system that protects both the human caretakers and the elephants, eliminates punishment and significantly contributes to the elephant’s psychological well-being. Positive control Positive control as practiced in a system of protected contact (PC) prohibits the elephant and the trainer from occupying the same space and places a barrier between them. Clearly, liability issues have driven much of the enthusiasm for PC training methods as many serious injuries and deaths are reported annually from elephant attacks (e.g., Priest 1992; Gore, Hutchins & Ray 2006). The crescendo of criticism by animal welfare and animal rights activists is often focused on aversive control methods. We are aware of one situation where a sanctuary adopted a combined “free contact/positive control” variation of elephant management. Under these conditions, keepers entered into FC with the elephants but did not carry an ankus or any other tool for protection. Evaluators for the AZA have warned that this practice is unsafe. This and other management idiosyncrasies have contributed to the AZA’s reluctance to utilize some sanctuary holding facilities. Tragically, the recent death of an employee at Hohenwald Sanctuary in Tennessee (Ammon 2006) demonstrates the danger of working in close, unprotected contact with elephants. According to the data examined by Gore, Hutchins and Ray (2006), the “greatest likelihood of being injured is when using the free/direct-contact system” (p. 60). Clearly, if keepers do not enter an elephant enclosure, they cannot be killed by them. AZA elephant guidelines have fallen short of an endorsement for the astute protected contact system. While some may argue it has not yet risen to the level of best practice, it is surely the safest practice. Currently, there are some zoos using a “hybrid” management system consisting of elements of both FC and PC. The hybrid approach enables keeper and medical staff to assist in complicated procedures associated with the birth process. Since elephants often have trouble expelling a newborn, human intervention is considered by many experts as a necessary practice to facilitate a healthy birth. Anesthesia is not an option in such cases. As births are uncommon in zoo elephants, it is unclear whether FC needs to be practiced on a daily basis. Moreover, by practicing both systems simultaneously, it is possible that some confusion (and error) will arise among both the elephants and their caretakers (e.g., Wilson, Bloomsmith & Maple in prep.). When managing other large, captive wildlife such as apes, bears, hippos, leopards, lions, tigers or rhinos, the overwhelming majority of American facilities handle them with PC training or other remote management techniques. In European and Asian zoos, large, dangerous animals are handled more frequently at greater risk to caretakers and veterinarians. Behavioral management/enrichment Since there is no feasible way to provide zoo elephants with the vast space of their wild counterparts living free in Africa or Asia, it is essential that they be provided sufficient opportunity to stay active and healthy by other means. Like apes and other zoo creatures, elephants can develop bad habits in restrictive enclosures and succumb to lethargy, obesity and poor health. We should look to activity metrics in the field to learn about the elephant’s optimal investment in locomotion. While we may not be able to match the optimum, we may be able to improve their health by inducing more episodes and greater durations of activity. Enrichment and behavioral management techniques are the best ways to address behavioral deficiencies in time and space. 140

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A wide variety of environmental enrichment techniques, devices and procedures have been developed and tested for nonhuman primates, and a similar protocol should be adopted for elephants. Various types of enrichment have been assessed to determine their effects on behavior, including feeding enrichment, enhancements to the physical environment such as objects and furnishings, sensory enrichment and occupational tasks that require the use of problem-solving skills (cf. Bloomsmith & Else 2005 for a review relevant to chimpanzees). Many enrichment procedures have been shown to have sustained positive effects on primate behavior. Others have not, but the most promising techniques have been incorporated into daily care routines in many zoos. In contrast, there have been very few enrichment studies of captive elephants (Wiedenmayer 1998; Morimura & Ueno 1999; Stoinski, Daniel, Liu & Maple 2000), with mixed results. Markowitz carried out a classic manipulation at the Portland Zoo where he installed an apparatus from a car-washing platform that was operated by elephants that pulled a chain to produce a shower on demand (Markowitz 1982). Further, the incorporation of innovative feeding techniques into elephant management can be used to elicit traveling, searching and processing food, all of which increase activity (Kinzley 2006). In the last two decades, the systematic application of operant conditioning has been widely applied to the care, management, exhibition and study of nonhuman primates, with a particular emphasis on the use of positive reinforcement techniques (Priest 1991; Forthman & Ogden 1992; Bloomsmith 1994; Pryor 1999). The field of research and relevant applications is collectively known as “behavioral management.” The systematic application of behavioral management fundamentals has changed the way many nonhuman primates have been handled, with less coercion and more reward. The change in procedures parallels the transition from FC to PC management systems that has taken place in many AZA zoos during the same general time frame (Bashaw et al. 1999). It is widely assumed that such training reduces physiological changes associated with stress, and that training animals to cooperate with procedures benefits their welfare by moderating individuals’ perceptions of stress during certain procedures (Reinhardt 1991; Koban, Miyamoto, Donmoyer & Hammar 2005; Lambeth, Perlman, Thiele & Schapiro 2005; Savastano 2005; Videan, Fritz, Murphy, Borman et al. 2005; Lambeth, Hau, Perlman, Martino et al. 2006). In addition to reducing distress, there are other applications of these techniques such as moderating social aggression (Bloomsmith, Laule, Alford & Thurston 1994) and increasing physical exercise. Elsewhere (Bloomsmith, Marr & Maple 2007), we have discussed the use of human training technology applied to nonhuman primate management, and we have proposed the use of operant training to control problematic behavior such as stereotyped behavior or self-injurious behavior, as has been quantitatively assessed in the human literature for more than four decades (e.g., Kahng, Iwata & Lewin 2002). We believe that this literature from the behavior analysis research community, based on human subjects, will be enormously helpful in developing effective training methods for preventing, ameliorating and treating stereotyped and self-injurious behavior in captive animals, and this opportunity should be investigated for elephants. The next generation of elephant exhibits There is a growing consensus among zoo biologists that we need to provide bigger and better zoo facilities for elephants. Indeed, as this chapter is being prepared, AZA has cited more than 50 projects currently underway or planned by AZA zoos that have committed to new elephant facilities (Maddy, pers. comm. 2006). The frenzy of planning and construction demonstrates that AZA zoos recognize deficiencies in their facilities. Building on these projects, the next generation of elephant exhibits will surely be comprised of the following programming elements: 1. Sufficient 141

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space to encourage locomotion, manipulation and social interaction, in all likelihood greater than five acres for a group of any size; 2. Management practices that encourage variable interval feeding, unpredictable distribution of food and browse, good nutrition (and weight control) and positive reinforcement training methods; 3. Species-appropriate, complex social groups and reinforced structures for the safe housing of breeding age bulls; and 4. Specialized caretakers with advanced training in the fields of animal behavior and/or behavior analysis. Future elephant exhibits will be designed with elephant welfare as a high programming priority. Naturalistic features will provide elephants with a soft, flexible, challenging environment. We predict a better future for captive elephants as zoos aggressively advance their operating and exhibition practices. The intent of zoo managers today is to restrict elephant exhibition to those institutions that meet the complex biological and behavioral needs of the species (e.g., Hutchins, Smith & Keele in press). Therefore, fewer zoos will exhibit elephants but those that do so will have to meet advancing, stringent and highly scrutinized standards of quality. To monitor performance, it is imperative that we develop animal welfare criteria based on an objective science of animal welfare (Maple 2007), and we must create appropriate evaluation metrics to protect the credibility of our recommendations. On issues such as “how much space does an elephant require in a zoo?” speculation, anecdote or opinion is not sufficient. We need data from carefully executed experiments and controlled systematic observation in order to reach valid, useful conclusions. While we have a wealth of data from nonhuman primate studies and these data have driven strong recommendations on housing and management, we will need a similar treasure trove of information to confirm new standards for elephants. However, there is already a sufficient quantity of evidence to expose the flaws and deficiencies in current facilities and standards, so it is safe to conclude that change is necessary. It is the degree or magnitude of change that is debatable. By increasing the designated area for zoo elephants, without reference to what happens in the expanded space, we will likely fail to improve their experience of captivity. Elephants will benefit from studies of systematic changes in spatial and management variables to determine what works. As new exhibits are constructed, a series of post-occupancy evaluations (Maple & Finley 1987) would be helpful. In the immediate short term, we recommend careful evaluation of the newest exhibit innovations in Cologne, Copenhagen, Oakland, North Carolina and other locations worldwide. Many zoos have been subjected to pressure from animal rights groups that want elephants removed to sanctuaries. The motives underlying this criticism are unclear, but AZA institutions believe that their most extreme and vociferous critics are seeking to shut down zoos, species by species. Rather than enter into a cooperative relationship to discuss elephant exhibit deficiencies, debate prospective solutions and then work together to implement them, some zoo adversaries have chosen to attack zoos in aggressive media campaigns, appeals to local government regulation and through litigation. A debate on elephant needs and requirements must be evidence-based, so it is important that zoos encourage and sponsor objective studies of the variables that affect the psychological well-being and health of elephants. It is puzzling that zoo professionals do not yet have a clear idea about the minimal effective space for captive elephants, nor do they have a policy on substrate and activity. Zoo standards must be defensible by the strength of the scientific data, and this is why active scientific programs are so critical to zoo management. One example is the recent paper by Wemmer, Krishnamurthy, Shrestha, Hayek, Thant and Nanjappa (2006) that developed a standard for judging the bodily condition of elephants. Their work, based on observations of Asian elephants, provides an objective standard that may be useful in making medical decisions. More research of this kind will be helpful to managers and veterinarians who have to make difficult 142

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decisions about when to intervene medically. It may also be useful to consider Maslow’s “hierarchy of needs” a construct modified for primates (Maple 1996). In theory, a hierarchy of needs exists for every species and is likely unique for each species. It may also vary according to the psychological makeup and social history of individuals. Research in this domain would help managers and caretakers to engineer appropriate physical and social environments. Avenues of constructive criticism The tactics of many animal rights and adversarial welfare interest groups have polarized zoo professionals and their critics, due, in part, to the perception that some of these groups are motivated primarily by their desire to abolish zoos. Constructive critics should clearly state their true intentions, and reach some accommodation with the institutions they are seeking to reform and improve. At the same time, AZA zoos need to reach out to field and zoo biologists outside the fraternity of zoos to prevent insular thinking and provide for open debate and discussion. This is particularly necessary in the field of animal behavior. In our opinion, every zoo and aquarium in the AZA, big or small, would benefit from the employment or close collaboration of a doctorallevel animal behaviorist. Behavior is the lynchpin of enlightened zoo management, and certified animal behaviorists on-staff can function as buffers and counterpoints to irresponsible criticism from extremists in the animal rights movement. In partnership with veterinarians, animal behaviorists ensure that animal welfare provisions will be a continuing priority within the institution. Grounded in methodology and statistics, animal behaviorists are also well-suited to a role as monitors of psychological well-being. Accredited zoos and aquariums are required to employ qualified part- or full-time veterinarians; we think they should also employ qualified animal behaviorists. Indeed, this is exactly what has happened over the last 20 years in laboratory facilities and primate research centers that house large numbers of nonhuman primates. Now, most major primate facilities employ doctoral-level behavioral scientists who guide and evaluate the behavioral management programs at these facilities (Baker, Weed, Crockett & Bloomsmith 2006) with the goal of promoting the psychological well-being of the nonhuman primates living there. In a recent address to the Animal Behavior Society, Robert Trivers (2006) remarked that the study of animal behavior offers “a guide to what is important in the animal’s life.” This is an eloquent rationale that zoo professionals should embrace and endorse. Since the publication of Ethics on the Ark (Norton, Hutchins, Stevens & Maple 1995), opportunities for debate and dialogue among zoo professionals, scientists and animal welfare activists have been few and far between (but cf. Beck, Stoinski, Hutchins, Maple et al. 2001). Meetings such as the 2005 Tufts Conference on “Elephant Science and Well-Being” must be inclusive if zoo managers and outside experts want to identify welfare principles that work in the zoo. If data fuel the debate on elephants in zoos, the community of scholars, managers and activists will doubtless reach consensus on the next steps to be taken. We need a detailed roadmap to help us improve elephant exhibits and elephant management in the zoo, but we should be careful to expend scarce resources on features that really matter. Exhibits in Los Angeles and Washington, D.C. respectively, currently in the planning stages, have been estimated to cost between 40 and 60 million dollars. Will these enormous sums bring innovation or more of the same? Creative designers and scientific programmers will need to think outside the box to satisfy the needs of earth’s largest land mammal. Two decades ago, in the rush to improve nonhuman primate facilities, scientists operationally defined “psychological well-being” and promulgated objective assessments for many species. Elephants will benefit from a similar comprehensive analysis. Since elephants are cohesive social creatures, a minimal standard of exactly “x” acres per elephant makes little sense. It may be preferable 143

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to consider “y” acres per group no matter their size. By this reasoning, 10 elephants may do quite nicely on a minimum of five to 10 complex, naturalistic, enriched acres of outdoor space. Similarly, Hutchins (2006) suggested four to seven acres would be adequate for a group of elephants. Careful planning is necessary to determine this arbitrary but effective unit of space. In addition, because elephants extend their reach with their lengthy trunks, it is appropriate to consider volumetric space when designing for elephants. They get plenty of exercise when they have to stand on their back feet and extend their trunks to reach edible material high above them. Clever and contrived zoo habitat functions in this way as the elephant’s own “impersonal (and inanimate) trainer.” If regulating experts should agree that any particular zoo facility is harmful to elephants, the animals must be provided an alternative, better exhibit or a retirement facility, but there is currently much disagreement about appropriate standards or best practices (see Kane, Forthman & Hancocks, eds., Appendix II), even in accredited zoos. Historically, AZA’s increasingly stringent accreditation standards have not been uniformly applied. Few empirical standards exist for any large mammals, so we are forced to compare apples to oranges, for example field norms to zoo norms. The provision of mean home range data or quantified daily travel patterns is useful in demonstrating an activity gap between captivity and the field, but it is not practical to replicate home ranges in the zoo. Enrichment can add hours to the activity budget of any zoo animal, so we can move captive behavior closer to the field standard if we engineer their schedule. Time spent moving is probably a more appropriate indicator of normal elephant behavior, so our task is to somehow activate elephants. Perhaps the best way to answer the looming question of whether elephants belong in the zoo is to proclaim “only active elephants belong.” This assertion could be the first point of agreement in a new paradigm for the behavioral management of elephants in the zoo. AZA intends to look more closely at elephant exhibit standards zoo by zoo during the accreditation process, an assessment that should be quickly and firmly implemented. Wellness and wildness It may be useful to interject the concept of “wellness” into the conversation on elephant welfare. Extending the ideas that are transforming human health to animals will require careful and critical analysis to identify those that may be universally applicable. Inducing activity through training is already practiced in accredited zoos and aquariums, although such programs are also valued because they provide entertainment to visitors. However, by contributing to wellness, defined in part by better physical and mental health, zoo managers serve a more compelling and nobler purpose. Every zoo animal would benefit from a wellness program tailored to its individual history and its needs. Wellness in human medicine equates to proactive, preventive and caring medical practice in the zoo, but it is as much a behavioral as it is a medical construct. Innovations in this domain should be encouraged with veterinarians consulting with psychologists, nurses and other medical personnel to find new methods to prevent obesity and promote fitness as measured and monitored by objective criteria. One way to advance wellness is to envision greater opportunities for wildness. In a classroom discussion with architecture and psychology undergraduates at Georgia Tech, we asked them to envision a wilderness park extending from the zoo to the northern Atlanta suburb of Buckhead, a distance of approximately 10 miles. The protocol called for the elephants to be dispersed at night and permitted to wander this green pathway to Buckhead and back to the zoo, a journey that would take many hours to complete. The managed “wilderness” concept of “Buckhead Elephant Park” was rendered by one of the students and depicted in Figure 3. Sometimes an arguably crazy idea, generated in the heat of a classroom discussion, is just what the doctor ordered. If implemented, 144

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Figure 3. Managed “wilderness” concept of “Buckhead Elephant Park”.

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the conceptual Buckhead Elephant Park, or something like it, would surely be recognized as an innovation in the promotion of wildlife wellness. Zoo professionals and experts in field biology and animal welfare have disagreed about many aspects of zoo elephant management and exhibition, but there is also growing agreement on key issues. We all agree that elephants need more space in the zoo, but we have not reached agreement on how much space is adequate or optimal. We all agree that elephants should live in social groups with as much age diversity as possible, but we do not yet agree on an appropriate number or standard of stratification. We all agree that elephants in the zoo need more exercise, and they need softer, more naturalistic surfaces to walk on and manipulate. We also agree that elephants need intellectual challenges in the zoo, comparable to the challenges they face in nature, for example, social complexity, opportunities to forage, variations in feeding schedules and interactive forms of enrichment. Most of us agree that elephants should be permitted opportunities for activity day and night, and most of us have agreed not to chain elephants nor control them with aversive, punitive training methods. We are encouraged at how much common ground has been identified, and we are hopeful that much more can be achieved in the near future. Acknowledgments We gratefully acknowledge continuous research funding by the Center for Conservation and Behavior at Georgia Institute of Technology, and the Elizabeth Smithgall Watts Endowment and the Charles Bailey Fund at Zoo Atlanta. The support of the Charles Schmidt College of Sciences and the Biology Department at Florida Atlantic University is also gratefully acknowledged. Dr. Bloomsmith’s nonhuman primate research is supported by Yerkes National Primate Research Center Base Grant RR-00165 awarded by the National Center for Research Resources of the National Institutes of Health. Ms. Martin’s work is supported by the Nelly and Geoffory Bourne Fellowship and the Yerkes National Primate Research Center Base Grant RR-00165 awarded by the National Center for Research Resources of the National Institutes of Health. The work reported herein was inspired by a white paper circulated by Lisa Kane and Debra Forthman during the period of Dr. Maple’s service as President of AZA, and written during his tenure as President/CEO of the Palm Beach Zoo. The manuscript was improved by critical comments provided by Debra Forthman, David Hancocks, Gary Lee and Keith Lovett. References

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Azrin NH. 1960. Effects of punishment intensity during variable-interval reinforcement. J Exp Anal Beh 3:123-142. Azrin NH, Hake DF, Hutchinson RR. 1965. Elicitation of aggression by a physical blow. J Exp Anal Beh 8:55-57. Azrin NH, Holz WC 1966. Punishment. In: Honig WK, ed. Operant behavior: areas of research and application. Englewood Cliffs, NJ: Prentice Hall. p. 380-447. Azrin NH, Holz WC, Hake DF. 1963. Fixed-ratio punishment. J Exp Anal Beh 6:141-148. Azrin NH, Hutchinson RR, Hake DF. 1963. Pain-induced fighting in the squirrel monkey. J Exp Anal Beh 6:620. Azrin NH, Hutchinson RR, Sallery RD. 1964. Pain-aggression toward inanimate objects. J Exp Anal Beh 7:223-228. Azrin NH, Ulrich RE, Hutchinson RR, Norman DG. 1964. Effect of shock duration on shock-induced fighting. J Exp Anal Beh 7:9-11. Azrin NH, Hutchinson RR, McLaughlin R. 1965. The opportunity for aggression as an operant reinforcer during aversive stimulation. J Exp Anal Beh 8:171-180. Baker KC, Weed JL, Crockett CM, Bloomsmith MA. 2006. Survey of environmental enhancement programs for laboratory primates. Am J Primatol 68:1-19. Bashaw MJ, Burks K, Daniel E, Maple TL. 1999. Environmental variables and the well-being of captive elephants. Proc Elephant Manager’s Association conf and the Fourth Int Elephant Research Symp. Atlanta, Georgia. p. 23-25. Bayne KAL, McCully C. 1989. The effect of cage size on the behavior of individually housed rhesus monkeys. Lab Anim 18:25-28. Beck BB, Power ML. 1988. Correlates of sexual and maternal competence in captive gorillas. Zoo Biol 7:339-350. Beck BB, Stoinski TS, Hutchins M, Maple TL, Norton B, Rowan A, Stevens EF, Arluke A, eds. 2001. Great apes and humans: the ethics of coexistence. Washington, DC: Smithsonian Institution Press. Bloomsmith MA, Else JG. 2005. Behavioral management of chimpanzees in biomedical research facilities: the state of the science. ILAR J 26:192-201. Bloomsmith MA, Pazol KA, Alford PL. 1994. Juvenile and adolescent chimpanzee behavioral development in complex groups. Appl Anim Behav Sci 39:73-87. Bloomsmith MA. 1994. Evolving a behavioral management program in a breeding/research setting. In: Proc ann conf AZA. p. 8-13. Bloomsmith MA, Laule GE, Alford PL, Thurston RH. 1994. Using training to moderate chimpanzee aggression during feeding. Zoo Biol 13:557-566. Bloomsmith MA, Marr MJ, Maple TL. 2007. Addressing nonhuman primate behavioral problems through the application of operant conditioning: is the human treatment approach a useful model? Appl Anim Behav Sci 102:205-222. Boren JJ, Colman AD. 1970. Some experiments on reinforcement principles within a psychiatric ward for delinquent soldiers. J Appl Behav Anal 3:29-37. Brockett R, Stoinski R, Black J, Markowitz T, Maple TL. 1999. Nocturnal behavior in a group of unchained African elephants. Zoo Biol 18:101-109. Buckley C. 2001. Captive elephant foot care: natural habitat husbandry techniques. In: Csuti BA, Sargent EL, Bechert US, eds. The elephant’s foot: prevention and care of food conditions in captive Asian and African elephants. Ames, IA: Iowa State University Press. p. 53-56. Burghardt GM, Ward B, Rosscoe K. 1996. Problems of reptile play: environmental enrichment and play behavior in a captive Nile, soft-shelled turtle, Trionyx triunquis. Zoo Biol 15:223-238. Buss IO, Smith NS. 1966. Observations on reproduction and breeding behavior of the African elephant. J Wildl Manage 30:375-388.

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Dr. Terry L. Maple is Elizabeth Smithgall Watts Professor of Conservation and Behavior and Professor of Psychology at the Georgia Institute of Technology. During the past three years he has worked as President and CEO of the Palm Beach Zoo on academic leave. His previous executive experience includes 17 years as President/CEO of Zoo Atlanta and one year on the staff of the Audubon Zoo in New Orleans. Dr. Maple is also the founding editor of Zoo Biology, and one of the founding members of the American Society of Primatologists. His books include Captivity and Behavior (1979), Orangutan Behavior (1980), Gorilla Behavior (1982), Zoo Man (1993), Ethics on the Ark (1995) and Saving the Giant Panda (2000). He is an elected Fellow of the American Psychological Association and the Association of Psychological Science, and a former President of the Association of Zoos and Aquariums. He may be contacted at Georgia Tech Center for Conservation and Behavior, School of Psychology, Georgia Institute of Technology, 654 Cherry Street, Atlanta, GA 30332-0170, at [email protected]; or at http://conservationandbehavior.gatech.edu. Dr. Mollie Bloomsmith is the Head of Behavioral Management at the Yerkes National Primate Research Center where she supervises the enrichment, socialization and animal training programs. She is also the Associate Director of the Center for Conservation and Behavior at the Georgia Institute of Technology. Dr. Bloomsmith conducts research to evaluate behavioral management and its impact on animal welfare in laboratories and in zoos, studying a wide variety of species. She may be contacted at Yerkes National Primate Research Center, 954 Gatewood Road, Atlanta, Georgia 30329, or at [email protected]. Allison L. Martin is a graduate student in the School of Psychology’s Center for Conservation and Behavior at the Georgia Institute of Technology. Ms. Martin received a BS in psychology from Kennesaw State University. She is a current recipient of the Nelly and Geoffory Bourne Fellowship. Her research interests include applied behavior analysis and behavioral management in a variety of species. She may be contacted at Center for Conservation and Behavior, School of Psychology, Georgia Institute of Technology, 654 Cherry Street, Atlanta, GA 30332-0170, or at [email protected].

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