Chapter 9 Unpacking the Trunk: Using Basic Research Approaches to Identify and Address Captive Elephant Welfare Concerns Joseph C. E. Barber Asking and answering questions is the foundation of scientific research. There are many questions about the welfare of captive elephants, but few answers, and much of the debate about the suitability of captive environments for elephant welfare could be better addressed if there were more objective data available. A recent petition submitted to the United States Department of Agriculture (USDA) Animal and Plant Health Inspection Service (APHIS-2006-0044) by the animal protection group In Defense of Animals (IDA) illustrates some of the key concerns that zoos, animal welfare organizations and opponents of elephants being housed in captivity are debating. Focusing on the potentially life-threatening issues of foot and joint disease in captive elephants, and suggesting that this is an indicator that current elephant care guidelines and standards are insufficient to meet their needs, IDA requested that the USDA/APHIS clarify the space requirements necessary for the physical health and psychological well-being of elephants in captivity. In response to this petition, APHIS sought public comment on this issue, and requested the following information (APHIS-2006-0044-0001): • What are the causes of arthritis in elephants? • What, if any, foot care practices have been used on captive elephants to maintain healthy feet? • What floors are best for captive elephants? Are there any flooring conditions that promote foot problems? • Do captive elephants require a certain amount of exercise (i.e. walking) to maintain healthy feet? • What industry standards are available for elephant care and husbandry? • Are there any other health or care issues related to elephants that should be specifically addressed in the Association of Zoos and Aquariums (AZA) standards? The goal of this chapter is to begin to prioritize the many questions asked about elephant welfare—based in part on the frequency with which they are asked by the diverse organizations interested in captive elephants. The expertise of animal care professionals will be used to compare the different approaches to elephant care taken by different regional zoo associations. Scientific questions from zoo and non-zoo scientists will also be examined, as will questions from nonzoo animal welfare organizations. The greater the consensus that groups with such wide-ranging 111

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opinions have on specific questions regarding captive elephants, the more likely it is that these questions will be important to our understanding of elephant welfare. Basic approaches to answering some of these questions will be suggested within this chapter. Review of zoo association guidelines and standards Zoos readily acknowledge that elephants require a significant investment of time, money and care to meet their needs in captivity. The British and Irish Association of Zoos and Aquariums (BIAZA) states that institutions unable to provide a high enough standard of care should not house elephants (Stevenson & Walter 2006). Many zoo associations such as BIAZA, the European Association of Zoos and Aquariums (EAZA) and AZA, as well as conservation organizations such as the International Elephant Foundation (IEF), have developed specific elephant care guidelines (and actual standards in some cases) to encourage consistent management practices that attempt to meet the needs of these animals. There is currently no single set of elephant care guidelines that is applied consistently throughout the different regional zoo associations, although the Elephant Husbandry Resource Guide (Olson 2004) is cited most frequently. Elephant care and management guidelines are based on a combination of scientific research and the practical experience of those who have worked with elephants for many years. These guidelines are reviewed and updated frequently, sometimes based on emerging scientific information from proactive research studies, oftentimes as a response to public or scientific criticism. Many scientists and professionals outside of the zoo community are concerned that zoo elephant guidelines and standards are not based on enough scientific research to be valid, and fail to take into account existing natural history research (e.g., Clubb & Mason 2002); and that they are—often admittedly—minimum, not optimum, standards of care. This chapter focuses on areas of inconsistencies between different regional zoo associations, and differences in opinions between zoo and non-zoo organizations, as to the most effective standards of care for captive elephants. This lack of agreement is often based on areas where there are insufficient objective data available to make clear recommendations, and where future research will be very valuable. The list of topics addressed in this review closely mirrors the sections used within zoo guidelines on elephant care (e.g., Stevenson & Walter 2006). These are not mutually exclusive categories. Welfare is influenced by the combination of these issues, not by any single one. Elephant behavior The significant amount of behavioral research on wild elephants is frequently cited within zoo guidelines. Wild elephants are active approximately 19 hours per day, spending 16 of these feeding and foraging—typically on the move (McKnight 1995; Vinod & Cheeran 1997; Reimers, Schmidt & Kurt 2001; Leggett 2006; Dai, Shannon, Slotow, Page & Duffy 2007; Lee & Moss, Chapter 2; Poole & Granli, Chapter 1; Williams, Chapter 3). Comparing the difference in activity budgets between wild and captive elephants is considered an indicator of how successful captive conditions are at meeting the needs of elephants (Stevenson & Walter 2006). All zoo guidelines agree that elephants need the opportunity to express species-appropriate behaviors. What is not well understood is which behaviors elephants are highly motivated to perform in captivity, and which are strongly motivated by internal factors, and so will be important to elephants even in the absence of appropriate external stimuli. What is known is that preventing animals from performing highly motivated behaviors can lead to the development of stereotypic behaviors (Wiedenmayer & Tanner 1995), frustration-induced aggression (Duncan & Wood-Gush 1972; Fraser & Broom 112

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1990; Broom & Johnson 1993) and reproductive suppression (e.g., Schulte, Feldman, Lambert, Oliver et al. 2000). Zoo and non-zoo organizations alike often cite the need to design captive environments that meet the needs (social, behavioral, physical, psychological, etc.) of elephants in captivity (Stevenson & Walter 2006; AZA 2007; Kane, Forthman & Hancocks, Appendix I). From a behavioral perspective, this requires identifying those behaviors that the elephants themselves find important (e.g., Mench & Kreger 1996, p.13; Clubb & Mason 2004, 2007) rather than arbitrarily choosing those behaviors on behalf of the elephants (perhaps based on the resources available at a captive institution). This is something that has not been attempted formally, and few of the published guidelines specifically address this issue. Indeed, studies that measure the “demand” that animals show to perform certain behaviors, based on the amount of effort or “cost” they are willing to endure, have typically not been performed outside of a controlled laboratory environment (e.g., Mason, McFarland & Garner 1998). While the research tools may exist for answering these types of questions (e.g., Cooper & Mason 2001), the practical application of these tools to species such as elephants, in facilities such as zoos, has yet to be attempted. The challenges of setting up such experimental studies are covered in more detail elsewhere (e.g., Kirkden, Edwards & Broom 2003; Cooper 2004), but include determining preferences of individual animals within social groups (Sherwin 2004) and measuring motivation for resources without providing sensory access to those resources (Warburton & Mason 2003). Social behavior and structure The question of social structure has been identified as a key issue of captive elephant welfare, based on the clear differences in the social structure of wild and captive elephants. In the wild, elephants form complex social relationships over extended periods of time, and maintain these relationships throughout their lives, despite changes in age or status (Payne 2003; Lee & Moss, Chapter 2; Poole & Granli, Chapter 1). The cohesion of the social herd is considered an essential component of an elephant’s life (Douglas-Hamilton & Douglas-Hamilton 1975; Eisenberg 1981; Moss 1988; Estes 1991, 1999; Sukumar 2003). Given the long lives of elephants and the significant change in captive management practices that have arisen over the last 30 years, many elephants now in captivity bear the legacy of what would now be considered by today’s zoos as outdated and inappropriate management. Many of the problems seen in the current elephant population (e.g., poor reproduction, aggression, social incompatibility) may be the result of a poor social and rearing environment decades earlier (Stevenson & Walter 2006), including conditions of capture, handling and transport prior to arrival at a zoo. While zoo guidelines often specifically state the need to replicate the social organization of elephants seen in the wild (Stevenson & Walter 2006), where finding groups of just two to three females would be very unusual (Poole 1994), the actual requirements or available facilities at zoos often fall far short of this goal. BIAZA and the Australasian Regional Association of Zoological Parks and Aquaria (ARAZPA) recommend a minimum of four females older than two years for each captive group of elephants (Standley & Embury 2004; Stevenson & Walter 2006), and AZA recommends a minimum of three females per group (cf. Olson 2004; AZA 2007). These minimum recommendations do not prevent zoos from maintaining social groups with larger numbers of elephants, similar to the average group size of more than 10 elephants (>five for Asian elephants) reported in the wild (Estes 1991; Sukumar 2003, p.172) and recommended by some elephant interest groups (Kane, Forthman & Hancocks, eds., Appendix II, S1-S3). However, these minima are based on a compromise between attempts at providing appropriate social groups in zoos, and 113

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the many challenges that most zoos would face if they had to house larger groups of elephants (Clubb & Mason 2002). Although the difference between a minimum of three or four elephants recommended by the different regional zoo associations is not large, the fact that different numbers are recommended reflects the mostly subjective approach taken by zoos in developing these standards of care. In many cases, the research has not yet been performed, or cannot yet be performed, because elephants have not been held in social groups much larger than those currently seen in zoos today, where housing only two or three elephants is common. Allowing olfactory and auditory communication among animals held in separate enclosures has been suggested as a possible way to expand the captive social environment, particularly for elephant bulls (Olson 2004), and even as a way to allow communication between elephant groups or individuals in different parts of the country (e.g., live transmission of sounds over the Internet between elephant facilities—G. Mason, pers. comm. May 16, 2006). No research has been performed to determine if this would be either an appropriate or effective addition to the social management of elephants, but replaying the sounds of conspecifics (especially unfamiliar ones) to other animals has been reported to be stressful if used in the wrong context (Volodina & Volodina 1999). Relatedness and social cohesion Individuals within wild elephant groups are very closely related (Archie, Moss & Alberts 2006; Couzin 2006), and maintaining a similar approach in captivity is thought to impart a considerable behavioral benefit (Schulte 2000). Intra-specific aggression is one issue identified by zoo guidelines that needs further investigation (Stevenson & Walter 2006). Possible causes of aggression within zoo elephant groups in captivity include creating unrelated groups of females, separating and reintroducing females from related groups for breeding transfers, and building small enclosure sizes and restrictive spaces that prevent normal social behaviors (Clubb & Mason 2002). Some of the other questions posed within the zoo guidelines ask about the influence that the relatedness of a group of elephants has on the health and psychological well-being of individuals within the group and on the level of social cooperation within the group (Stevenson & Walter 2006). There is currently no elephant research in zoos that shows whether social groups made up of related individuals experience fewer aggressive interactions than those composed of unrelated individuals, and no definitive evidence shows that females living with related conspecifics will experience fewer problems at parturition (e.g., maternal neglect, aggression: Veasey 2006). Much of this research has yet to be performed simply because the elephant population in captivity is currently not large enough to provide sufficient variation in management approaches (e.g., group sizes) for this to be feasible. Until there are changes to the housing and management of elephants within zoos that allow larger groups of related individuals to remain together, it will be difficult to answer these questions. The role that matriarchal-type females play in maintaining social cohesion within captive groups is understudied (Stevenson & Walter 2006). In the wild, matriarchs are usually the oldest, largest females who choreograph the daily routine of the herd (Moss & Poole 1983; McKnight 1995; Payne 1998). Reproductive success may even be improved in groups led by older matriarchs (McComb, Moss, Durant, Baker et al. 2001). No research has been performed to determine whether captive herds are similarly led by matriarchs, whether a similar knowledge is (or can be) amassed by matriarchs in captive environments, and whether groups led by a specific matriarch are more successful. Zoo caretakers may often have a sense of which animal assumes a matriarch-like role, but there is an opportunity for more specific research to be performed. Multi-institutional 114

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research studies may be able to determine the effect that group relatedness has on matriarch formation, and how matriarch formation influences social cohesion. Elephant separations Questions about the appropriate timing of elephant separations have also arisen in zoo guidelines. Some state that the separation of females from established groups is necessary for genetic management of the captive population (Olson 2004), while others recommend that social groups remain undisturbed whenever possible (e.g., Stevenson & Walter 2006) and that males instead be moved to groups of females. Non-zoo guidelines state that in the absence of exceptional circumstances, female calves should never be separated from their mothers (Moss 1988; Estes 1991, 1999; Taylor & Poole 1998; Clubb & Mason 2002; Kane et al., eds., Appendix II, S3) and that related females should never be separated from each other (Kane et al., eds., Appendix II, S3). This reflects conditions typically seen in the wild (Moss 1988). There is a general acceptance within the zoo community that transferring females is currently still part of elephant management (although moving gametes instead of elephants may be a viable alternative to moving and separating animals if assisted reproductive technology is used), and so zoo guidelines also provide specific recommendations for the separation of juveniles (males and females) from their herd. It is stated that juveniles should not be transferred from their herd prior to five years of age (Stevenson & Walter 2006) or prior to three years (AZA 2007), to ensure the appropriate behavioral development of the animals. Once again, these differences suggest an absence of objective research on the influence of separating elephants at a range of ages, not only at the time of separation, but also on the future health and reproductive success of the juveniles when they become adults. Clubb and Mason (2002) provide a summary of some of the effects that early or premature weaning or separation can have on the welfare of mammals in general, including impaired reproductive performance and the development of abnormal behavior as adults. It may be possible to look at this issue in elephants in captivity using pre-existing data in studbooks and from the behavioral observations performed on elephants in other zoo studies. Male and female interactions The social housing of males with other males and females is an area that requires further research (Clubb & Mason 2002). There is evidence to suggest that bulls, females and calves in captivity benefit from social interactions with one another (Sukumar 2003). Females that have had some form of experience with males during their lives are reported to be more sexually receptive to bulls, while females that have never seen bulls are reported to be more fearful, at least initially (Olson 2004). Within laboratory-housed, social species, the complexity of the social environment (e.g., group composition and stability, previous social experience) has been identified as a key element influencing behavior and welfare (Olsson & Westlund 2007). More research is needed to determine whether the interaction of males and females will affect long-term breeding success and social behavior in elephants too (Olson 2004). Some research suggests that elephant exhibits should be designed to allow free contact between male and female elephants throughout the day and night, while providing opportunities for elephants to avoid social interactions when they choose to do so (Glickman & Caldwell 1994; Forthman, McManamon, Levi & Bruner 1995; Rees 2001). Elephants lacking this social control may experience a significant decrease in their reproductive success (Freeman, Weiss & Brown 2004). Differences in the success of matings primarily initiated by females, compared to those primarily initiated by males (Poole, Taylor, Fernando, Ratnasooriya et al. 1997), suggest 115

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that mate choice is an important area of future research. Preliminary research has also shown that conception success is improved in captivity if bulls and cows are able to interact freely, and if cows are maintained in stable social groups (Kurt & Hartl 1995). Opportunities for males and females to interact for 24 hours throughout the estrous period have also been shown to increase the rate of pregnancy (Olson, Keele & Tuttle 1994). Multi-male groups An emerging management issue, in light of the zoo community’s greater desire for elephant reproduction (Olson 2004), is a lack of space to house males within current exhibits, especially if facilities choose to house males individually. This challenge is not unique to elephants, and many other species with social groups based on harems or multi-female groups face this issue in captivity. The idea of housing bachelor groups of males in single exhibits is one possible solution (Taylor & Poole 1998; Olson 2004; Stevenson & Walter 2006). Currently, the feasibility of this management approach is unknown. Since male elephants are often reared differently from females, and between institutions, determining what influence rearing environments (e.g., physical facilities, proximity of male and female conspecifics, training approaches) have on male sociability is an important question (Schulte 2000). Rearing young bulls in the presence of adult males may be important to minimize negative behaviors such as aggression (Schulte 2000; Olson 2004). The possibility that more dominant males may exert social control of musth behavior in juvenile males has also been raised (Taylor & Poole 1998; Slotow, Van Dyk, Poole, Page et al. 2000; Druce, Pretorius, Druce & Slotow 2006). It is not known whether housing two or more bulls in the same (or adjacent) enclosures influences the behavior of these animals, whether there are dominance issues, and whether this will ultimately affect the reproductive physiology of the animals (e.g., poor sperm quality) or promote subtle competition that will improve reproductive success (e.g., Keele 1996; Poole et al. 1997; Schulte, Freeman, Goodwin, Hollister-Smith et al. 2007). If zoos are to increase elephant reproduction, then the issue of housing multiple males should be addressed long before the time comes when this is actually needed (Veasey 2006). If gorillas are used as a model (Maple, Bloomsmith & Martin, Chapter 10), then there are many challenges that must be overcome when housing all male groups (e.g., Stoinski, Hoff, Lukas & Maple 2001; Stoinski, Lukas, Kuhar & Maple 2004a). Taking a more proactive approach by performing controlled research studies, such as looking at the introduction of male gorillas (e.g., Burks, Bloomsmith, Forthman & Maple 2001), and their long-term management (e.g., Stoinski et al. 2004a; Stoinski, Lukas, Kuhar & Maple 2004b), will be critical to prevent future welfare issues. Reproduction Reproduction is a key goal of most zoo elephant programs, as there are concerns about the sustainability of captive populations (Olson & Wiese 2000; Olson 2004). The premature onset and cessation of reproductive maturity has been identified as a priority issue for elephant research in zoos (Stevenson & Walter 2006). Large numbers of reproductively mature females in the captive population show no reproductive cycles (Olson 2004), and ovulation may be inhibited by social, nutritional and physiological stressors within the captive environment (Laws & Parker 1968). There are currently no recommended husbandry practices within zoo guidelines that address acyclicity in females (Olson 2004), and the results of reproductive studies (e.g., Freeman et al. 2004) are not yet transferable into specific management recommendations. As female elephants in zoos (especially those giving birth for the first time) have been known 116

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to injure or even kill their newborn calves under certain conditions, recommendations are made in zoo guidelines that females be separated from the herd (at least physically) and tethered (also known as chaining) during the first signs of labor, and the calf removed so that it can be reintroduced to the mother under more controlled conditions (Olson 2004). Few published investigations are available on the conditions needed for a successful captive birth within a social group as an alternative to this. While it is likely that social separation, chaining and calf reintroductions have reduced the risk of harm to calves born to females with behavioral problems or from abnormal rearing environments, the procedure inhibits the normal social bonding within elephant herds after birth (Estes 1991); it also prevents the directed investigation of the calf by other females that may be critical to their own future reproductive success (see similar issues with hand-rearing of gorillas: Meder 1989). If improvements are made to the social management of elephants—as partially recommended by the zoo guidelines reviewed herein—then it will be important to determine the long-term effects of this intervention management during birth. A risk/benefit analysis of natural, social births and subsequent interaction with the entire elephant herd will be needed, especially with the proposed increase in reproductive output within captive elephant populations. Assessing the influence that the relatedness of the herd has on the success of natural/social births would also be interesting. Health and nutrition There are currently no published records that quantify the incidence and severity of common elephant health issues, such as foot and joint problems, throughout the global captive elephant collection (Stevenson & Walter 2006). Few studies have been performed to investigate the influence of possible causative factors for these health issues, such as amount of time spent standing on hard substrates (e.g., Hittmair & Vielgrader 2000; Meller, Croney & Shepherdson 2007), nutrient deficiencies, excessive body weight or temperature. It is suggested that a lack of exercise and the heavier weights of captive elephants may lead to an increased prevalence of medical issues such as arthritis (West 2001; Clubb & Mason 2002), and the link between health and weight is well studied in farm animals (Webster, Knott & Tarlton 2005). Zoo guidelines identify obesity as a common issue for elephants in captive conditions (Stevenson & Walter 2006; AZA 2007), and also link obesity to issues such as poor reproductive success in males and females, dystocias and stillbirths (Kurt & Mar 1996; Olson 2004). More research has been called for to determine the role of obesity on elephant health (Csuti, Sargent & Bechert 2001; Hatt & Clauss 2006; Stevenson & Walter 2006). Circulatory problems have been identified as the most common cause of death in zoo elephants (Clubb & Mason 2002), and, given the association between circulatory disorders and factors such as obesity (Abate 2000) and chronic stress (Drolet, Beaulieu, Mansi, Champagne et al. 1995), this issue requires urgent investigation. Physical environment The space provided to elephants has been the subject of great debate and great controversy. Space is one factor that can be severely limiting within a zoo environment, although space is not just a single variable. Captive environments are multi-dimensional, and involve not only the physical parameters of the enclosure, but also aspects such as olfactory and auditory stimuli, variability and the overall physical and temporal complexity of the environment—all as perceived from the animals’ point of view. In general, environments provided to elephants in zoos should ensure that the animals have some element of control over their environment, being able to use their physical and behavioral adaptations to cope with the various challenges of the captive environment (e.g., 117

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presence of visitors, social stressors, weather conditions, etc). Control has been identified as a key component of welfare in many species (pandas: Owen, Swaisgood, Czekala & Lindburg 2005; rodents: Balcombe 2006; polar bears: Ross 2006; primates: Bassett & Buchanan-Smith 2007). Clubb and Mason (2002) were unable to find studies that specifically examined the influence that enclosure size has on elephant welfare, whether looking only at zoo enclosures, or comparing zoos with more extensive captive situations (e.g., sanctuaries, timber camps). Research from the zoo community has focused on more subjective evaluations (e.g., surveys of management approaches), and this has its drawbacks. For example, Hutchins (2006) states that elephants within AZA institutions “…seem to be doing just fine based on any objective measure of welfare one chooses, including successful reproduction, activity patterns, lack of stereotypic behavior, and animal health and mortality” (Hutchins 2006, p. 165), but there are few objective data to support this statement, and plenty of information that is available to refute it (much of which is equally subjective, however). None of these objective measures has actually been utilized within a formal study looking at group size, space, the nature and complexity of the space and welfare. Even identifying animal welfare “red flags” within the elephant population (e.g., foot and joint problems, development of stereotypic behavior) would be a much-needed, and more objective, approach to detect current trends within the population. A comprehensive, community-wide approach is also needed that tests specific predications and hypotheses about space, complexity and welfare. Exhibit sizes Within most zoo guidelines, exhibit size requirements are often stated as minimum sizes, and institutions are recommended to design exhibits larger than the minimums. For outdoor elephant exhibits, BIAZA guidelines recommend at least 2000m2 for up to eight female elephants (Stevenson & Walter 2006), while the AZA currently recommends 752m2 for eight elephants (AZA 2007), based on 167m2 for one elephant, and 83.6m2 for each additional elephant. Recommendations for mixed herds of bulls and cows are for exhibits no less than 3000m2 (Stevenson & Walter 2006). The minimum recommended space for indoor holding exhibits is 200m2 (Stevenson & Walter 2006) or 150m2 (AZA 2007) for four elephants. These recommendations within the zoo guidelines are not explained in any detail, and no information is provided as to how these sizes are calculated. Many exhibits will exceed these recommendations, but some will only just meet them. The different minimum standards recommended by the regional zoo associations again represent a lack of objective data on the influence that exhibit size actually has on the welfare of captive elephants. Some attempts have been made at creating more objective space recommendations by applying basic metrics to the calculations. The BIAZA guidelines for indoor exhibits are based on the stated need for elephants to “move and turn and lie down” (Stevenson & Walter 2006, p. 41), which is similar to the recommendation made for the care of farm animals reared within intensive farming systems, such as battery chickens (Brambell 1965). This approach does not address the wide range of species-appropriate behaviors that elephants may be motivated to perform. Kane and her colleagues (Appendix II) recommend that an indoor holding area for overnight housing should be at least 60m2 for each female elephant. This value was calculated by determining the space required for an individual elephant to sleep without lying in its own waste. Although this calculation does not specifically take into account other behaviors that elephants may be motivated to perform during the night, such as feeding and foraging (Brockett, Stoinski, Black, Markowitz et al. 1999), it represents one of the few attempts at a more objective approach to calculating space recommendations. Considerations of how much space elephants need to perform a wider range of behaviors (e.g., Stricklin, de Bourcier, Zhou & Gonyou 1998), and the influence that inter118

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individual distance and socially facilitated behavior have on these space requirements, are clearly important. Enclosure complexity and elephant health Zoo guidelines acknowledge that elephants in the wild do range over long distances (e.g., 8-22 km daily: Sukumar 2003; Stevenson & Walter 2006) and research has identified average daily traveling distances for elephants as 3.2 km (Asian female groups: Easa 1992; Reimers et al. 2001), 12 km (African female herds: Wyat & Eltringham 1974) and 8.9 km (Asian male elephants in musth: Sale, Chaudhury & Khan 1992; Reimers et al. 2001). Recommendations in non-zoo guidelines state that elephants should be able to roam at least 10 km (seven miles) per day while engaged in species-appropriate behaviors (Seidensticker & Doherty 1996; Hancocks 1996, 2002; Kane et al., eds., Appendix II, O1-O2). Health and reproductive problems are documented in elephants leading a sedentary lifestyle in zoos (e.g., Mikota, Sargent & Ranglack 1994; Csuti et al. 2001; Fowler 2001). Currently, zoo guidelines do not provide specific recommendations for the distance that elephants should travel each day. There is no magical number that will be appropriate for all elephants in zoos, but it remains important to compare the amount of space utilized by elephants with the prevalence of foot and joint issues, weight, opportunity to perform speciesappropriate behaviors and intra-specific aggression. It should be noted that the actual distance traveled by elephants in captive environments may be very different from the total distance that the elephants could travel within their enclosure, if, for example, resources were distributed or provided differently (e.g., Kinzley, Chapter 12). Nighttime and winter enclosures Within the BIAZA guidelines, it is stated that elephants benefit from having round-theclock access to outside enclosures (Priest, Antrim, Gilbert & Hare 1994). The need to house elephants indoors over night, and the design of traditional night housing with individual stalls for the elephants, has been shaped by the risk of aggression between individuals (Brockett et al. 1999; Stevenson & Walter 2006), as well as a concern for the safety of zoo staff and the public. General observations reveal that elephants in captivity can be active for more than half of the nocturnal period (Brockett et al. 1999; Weisz, Wuestenhagen & Schwammer 2000). Given the opportunity, this activity includes foraging and feeding, and the normal range of social interactions that would be observed during the day (Dai et al. 2007). Some elephant facilities use community stalls for housing elephants at night. Chaining is described within zoo guidelines as an acceptable form of elephant management if aggression or severe competition is seen within a herd housed overnight in these types of community stalls (Olson 2004). However, research has shown that chaining can lead to the development (or increased performance) of stereotypic behavior (e.g., Brockett et al. 1999; Gruber, Friend, Gardner, Packard et al. 2000). Chaining restricts simple locomotion within the indoor environment, but also prevents elephants from performing a wide range of other species-appropriate behaviors (e.g., grooming, foraging, social interactions, etc). Research has been performed on social preferences within elephant herds in captivity (Leong, Burks, Rizkalla & Savage 2005; Soltis, Leong & Savage 2005a, b), and such an approach may be a useful tool to understand how chaining may affect the complex social interactions of captive elephants. Given the clear curtailment of choice and control that elephants experience when chained, and the well-documented effects on animals lacking control within captive environments (Joffe, Rawson & Mulick 1973; Davis & Levine 1982; Mineka & Henderson 1985; Friend 1991; Ross 2006; Bassett & Buchanan-Smith 2007; Bradshaw, Chapter 119

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4), zoo elephant guidelines have begun to address this issue by recommending shorter periods of chaining where possible (<3 hours: Stevenson & Walter 2006; <12 hours: AZA 2007). Since there are objective data available on the effect that chaining has on behavior (e.g., Brockett et al. 1999; Gruber et al. 2000), these data should be used to make more informed recommendations on chaining. Addressing the social structure of elephants to minimize aggression and competition within groups, and to maximize the relatedness of individuals within groups, as some zoo guidelines are now recommending, may be an important additional step in addressing this issue. Elephants are not only housed indoors at night, but are also housed indoors by some facilities for periods during the winter in order to meet temperature recommendations. Zoo guidelines typically recommend different management approaches for indoor enclosure areas, especially those used for temporary periods (e.g., at night, during the winter). However, the needs of the animals do not change because they are housed indoors, and it remains important that the animals have the same behavioral opportunities inside as they would normally do outside (e.g., Seidensticker & Doherty 1996; Shepherdson 1998; Swaisgood, Ellis, Forthman & Shepherdson 2003). Research topics and approaches The goal of all animal welfare research must be to identify the specific needs of individual animals in confinement from a social, physical and psychological perspective. This research is essential as the management of elephants in zoos directly influences their physical health, behavior and physiology for the duration of their lives (Veasey 2006). Within the zoo and non-zoo guidelines reviewed above, physical space and the social environment stand out as key research priorities (Clubb & Mason 2002; Stevenson & Walter 2006; Kane et al., eds., Appendix II, Parts 2, 4, & 5). The following discussion describes some additional research approaches or models that may address these particular subjects, as well as their associated roadblocks. Understanding the effect that physical space and social environment have on elephants can be accomplished through a broad evaluation of the welfare of elephant groups in zoos. However, there is no single measure that can be used to assess animal welfare (Mason & Mendl 1993; Fraser 1995), as welfare focuses not only on the health of the animals (Dawkins 1998, 2004), but also on their subjective emotional experiences and perceptions of their environment (Dawkins 1990). While clearly linked, these two aspects of welfare do not always co-vary (Rushen 1991, 2003; Mason & Mendl 1993; Lane 2006). A wide range of measures is needed to build a picture of what elephants are experiencing in their captive environment. These measures can include behavioral time-budgets, reproductive success, occurrence of disease or injury, adrenal activity and level of immuno-suppression, to name a few. Some studies have already been performed that combine behavioral (e.g., stereotypies, activity budgets) and physiological (e.g., cortisol) assessments to measure aspects of elephant welfare (e.g., Dathe, Kuckelkorn & Minnemann 1992; Brown, Wemmer & Lehnhardt 1995; Clubb & Mason 2002; Wilson, Bloomsmith & Maple 2004; Kane et al., Appendix I), but the number is still small. One possible reason for a lack of substantive research on elephants may be the small elephant population available within the zoo community. The population of elephants in zoos is small, the number of elephants within each institution is also small, and rarely can single institutions create a representative sample of the entire elephant population in small-scale studies. When using inferential statistics, the small sample of animals used within a study should represent the much wider population (of elephants in captivity, in this case). Finding a representative sample, given the wide range of physical environments and management styles experienced by elephants in zoos, is very 120

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difficult (Kuhar 2006). Even when there is a large group of elephants at an institution, the animals are generally managed as a single group in a single enclosure; because each individual elephant is not independent from other group members, many statistical tests require that the group be counted as a single sample point (Plowman 2006). A strict interpretation of statistical assumptions is not always necessary (and has not stopped the publication of much useful research on captive animals), but the renewed focus on the use of randomization tests may provide a helpful tool to determine statistical significance when dealing with small sample sizes or individual animals (Todman & Dugard 2001; Plowman 2006). Statistical tests are not always used in captive elephant research. In many cases, more informal surveys are used to gather information. For example, an exhibit size survey might ask institutions to describe the amount of space given to the elephants and then list the prevalence and severity of foot and joint issues in the population. This type of “fishing expedition” survey is generally effective at seeing whether there are any obvious trends in the data that could be explored further, if reporting is done consistently and accurately. Identifying which elephants do not suffer from major issues, and examining the environments in which they have been managed, will also be useful in pinpointing best practices. A combination of informal surveys and more formal research studies has been very successful at identifying the needs of polar bears across a wide range of different institutions (Shepherdson, Carlstead & Wielebnowski 2004). However, “fishing expeditions” are limited— they only look at the conditions currently provided to elephants. If existing enclosure sizes are themselves subjective attempts at meeting the needs of the animals (i.e. not based on objective data relating to the natural history of the animals), then these types of research may not yield much useful information. Only through specific hypothesis testing will it be possible to generate the type of data necessary to develop species-appropriate management guidelines. Setting up a comprehensive program of hypothesis-driven environmental and management manipulations will be an important next step to take with elephant research in captivity (Wilson et al. 2004). While hypotheses can and should be developed based on information gathered from how elephants are currently exhibited, what is done now should not be the only source of information. Testing the hypothesis that elephant health will be maintained or improved if they are encouraged to walk at least five km per day by the spatial and temporal distribution of resources in the enclosure—and with that five km based on distances walked in the wild, for example—would be a more proactive approach than merely measuring how a two-acre exhibit affected foot and joint health, where the two acres provided to the elephants were simply all the space available, and where no attempt was made to assess distance traveled or time spent moving (e.g., Forthman et al. 1995). As an example of this hypothesis-testing approach, based on an understanding of elephant social behavior, two different types of introduction protocols for African elephants were tested to determine which was better at managing aggression and minimizing stress (Burks, Mellen, Miller, Lehnhardt et al. 2004). Another model for developing testable hypotheses, based on information initially gathered on current elephant environments in zoos, is research performed on clouded leopard exhibits (Wielebnowski, Busso & Brown 1999; Wielebnowski, Fletchall, Carlstead, Busso et al. 2002; Wielebnowski 2003). Multiple regression analyses have been performed between specific management practices (e.g., exhibits of specific heights/sizes) and indicators of welfare (e.g., cortisol) to look for trends or patterns; significant correlations have then helped in the development and testing of new welfarefocused exhibit designs (Wielebnowski et al. 2002). The drawback to this research approach is the time it takes for hypotheses to be supported or refuted. Management changes implemented today (e.g., different flooring types or exercise regimens) may not have a measurable influence on 121

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the foot health of elephant calves for 20-30 years. Moreover, for elephants showing foot and joint diseases, stereotypic behavior or bouts of aggression, there may be only a limited effect that certain management changes will have on these issues once they have become established. The goal must be to prevent these issues arising in the first place. Zoo associations face a significant challenge to meet the needs of elephants because of the limitations of money, space and other resources. The question remains whether zoos believe that they can (or should) attempt to optimize the welfare of their animals within the constraints of their facilities, or whether attempts should be made to eliminate these constraints and maximize the effectiveness of captive management protocols by testing novel approaches. Comprehensive research programs Olson (2004) identifies limited resources (e.g., lack of elephants, staff, researchers and funding) as one reason why there are still many unanswered questions about captive elephant care, but also admits that there has been no community-wide, comprehensive program of research for elephants to date. She recommends that a database of current elephant research be established, not only listing research that has been performed, but also research that needs to be performed. In their detailed report on elephant welfare, Clubb and Mason (2002, p. 250) reach a similar conclusion: “There is clearly an urgent need for a detailed, statistically sophisticated multivariate study of factors affecting elephant welfare.” With the public focus on elephants, it might be expected that there would be a similar research focus. However, performing and publishing research on these sensitive issues may be more challenging in an environment where both opponents and proponents of elephants being in captivity draw conclusions about the welfare of elephants based on very preliminary data, or on results that require further validation. Over-interpretation of single studies is unwarranted, and the process of data collection must continue until a clear pattern emerges. Moreover, if institutions are hesitant to perform research that shows potentially negative results because they fear the possible adverse press this research might generate, then reaching a point where elephants are provided with appropriate management—or the point where enough research shows that it may not be possible to care for elephants successfully in captivity—will remain unlikely. Making premature conclusions based on insufficient data may actually lead to adverse effects on the animals’ welfare—even with the best of intentions (Dawkins 2004). Conclusions The purpose of this chapter was to identify some of the main issues relating to the management of elephants in zoos, from both the public and scientific perspectives. Although many of the recommendations identified within the elephant guidelines developed by different regional zoo associations (e.g., AZA, BIAZA, EAZA, ARAZPA) are similar, there are notable differences. These differences highlight the lack of consensus between captive elephant experts on the most effective management protocols to ensure the welfare of elephants—and can be attributed to a lack of specific scientific information available. Creating objective, evidence-based standards of care will always be a complex task for any animal species in captivity, given the multi-factorial nature of the environment, and the complexity of animal welfare (Veasey 2006). However, the reliance on experiential standards of care by zoos, as a foundation for the welfare of elephants in zoos, remains an issue that will continue to promote much discussion. 122

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The elephant community as a whole must address the criticisms it faces and the management challenges of which it is already aware, and small-scale research projects must be combined with much larger-scale, multi-institutional studies (Schulte 2000), even though there are many challenges to setting up this type of research (Swaisgood & Shepherdson 2005). With successful multi-institutional studies already performed on several species (e.g., polar bears, rhinos, gorillas, clouded leopards), and refined research approaches available to address the statistical challenges that researchers face (e.g., Kuhar 2006; Plowman 2006), there is a great opportunity to improve our understanding. The most important next step will be to go ahead and actually perform the research. Acknowledgments I thank Dr. Jill Mellen for her valuable feedback on the drafts of this paper, Dr. Debra Forthman for her editorial encouragement and all reviewers who provided comments. References

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Dr. Joseph Barber received his Ph.D. from the University of Oxford, focusing on animal welfare in farm animals. After a joint post-doc at the University of Central Florida and Disney’s Animal Kingdom, as the Enrichment Research Fellow, Joseph took on the role of facilitator of the Association of Zoos and Aquariums’ (AZA) Standardized Guidelines project (now “Animal Care Manuals”), assisting in the development of animal care guidelines and recommendations for all bird and mammal groups within AZA animal collections. Joseph is an active member of the AZA Animal Welfare Committee and remains committed to making animal welfare a priority through his consulting work and graduate teaching. He may be contacted at 436 East Allens Lane, Philadelphia, PA 19119 or at [email protected].

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