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An Elephant in the Room: The Science and Well-Being of Elephants in Captivity

Paul F. Waldau North Grafton, MA, USA Lisa F. Kane Boulder, CO, USA Debra L. Forthman Atlanta, GA, USA and David Hancocks Melbourne, Victoria, Australia

A debilitating polarization prevails in our societys discussion of humans relationship to other animals and the natural world. The nonhuman world or what some call the more-than-human world (Abram 1996) is viewed in diverse ways. Some hold it to be merely a passive resource for our species benefit; others actively vilify it as full of vermin and dangerous animals that must be dominated or eliminated; still others romanticize it, holding our relationship to be, as Thoreau said in his essay Walking, the preservation of the world. Since the beginning of the 21st century, Western societys collective awareness of the influence of human activities on environmental degradation and loss of biodiversity has advanced dramatically. Many scientists have known for decades, even centuries, that our destruction of local habitats of nonhuman communities is dangerous. Yet, despite growing concern for humans effects on the majority of organisms, our global climate, and, indeed, the health of the Earth, there remains a bedrock of anthropocentrism among consumers and commerce that reinforces long-term habits of resource extraction and development, all of which discourage admission of the staggering environmental damage that humans have done, are doing and indubitably will continue to do in the future. One result of our species abuse of the planet is the extinction, and threat of extinction, of many nonhuman animalsparticularly those perceived to be either mere resources or competitors for resources regarded as ours alone. Keystone species and large animals are particularly vulnerable. Our deleterious influence is so significant that paleontologist Niles Eldredge of the American Museum of Natural History, who has compared the enormity of the five known previous extinction events to the effects of humans in recent time, has described the present global events as The Sixth Extinction. It is beyond debate that unless the current course of events is halted, elephants, whether in the wild or in captivity, will fall victim to The Sixth Extinction. The Proboscids have fallen from about 170 species to three during the Cenozoic era, with many members of the elephant family disappearing in surprisingly recent times, very possibly at the hand of humankind. The three remaining elephant species will only avoid this fate if we give them the urgent attention they require. This book and the conference from which it emerged was one effort to define the issues of
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paramount importance to their continued survival. The balance of this introduction describes: The meeting at Tufts Universitys Cummings School of Veterinary Medicine, out of which this book grew; The book itself; Potential influences of the book on Best Practices for elephants in captivity. The Tufts symposium These essays resulted from a gathering entitled A Symposium on Captive Elephants: Science and Well-Being. This two-day conference held in April, 2006 at the Tufts Center for Animals and Public Policy demonstrated clearly why discussion of the central, difficult issues raised by elephant captivity is necessary and important. The mission of the Center is to provide rigorously scientific and ethically sensitive analyses of past, present and possible future treatment of nonhuman animals. Its work is predicated on the tenet that animals matter in and of themselves. The Center recognizes that human and animal wellbeing is linked, and that both are improved through enhanced understanding of their interactions. The Coalition, a broadly based group, came into being in 2004 with the purpose of gathering, analyzing and disseminating science-based best practices to promote elephants biophysical, social and psychological welfare in captivity. This Symposium was one in a recent history of efforts to define the terms of the threats to elephants survival and to identify remedies that might guide our efforts to support the species robust success now, and perhaps for generations to come. We were particularly interested in exploring the effects of the biophysical and social environment on elephants that are managed closely. The Tufts Symposium was held precisely to bring together people with varied experiences and views about elephants in captivity. The meeting was deliberately as small as elephants are large, with invitations that nevertheless encompassed a diverse group of individuals. It was convened at a time when discussions by interested parties holding differing opinions about elephants in captivity have become virtually taboo. Such controversy is not uncommon these days; many discussions about humans relationships with wild animals are characterized by language that betrays deep, mutual mistrust. All too often, anyone who disagrees with or merely challenges one partys analysis of the crisis is subjected to harsh criticism. We were interested in achieving perspective, cooperation and, above all, potential solutions to the very complex problems involving captive elephants. Unfortunately, not all of those invited accepted, particularly some who are prominent in the zoo industry. In fact, some opposed the conference so strongly that they worked to have it canceled. One could view this state of affairs in terms of endocrinologist Hans Selyes general adaptation syndrome, in which he described three universal stages of coping: First there is an alarm reaction, in which the body prepares itself for fight or flight. No organism can sustain this condition of excitement, however, and a second stage of adaptation ensuesIn the second stage, a resistance to the stress is built. Finally, if the duration of the stress is sufficiently long, the body eventually enters a stage of exhaustion, a sort of aging due to wear and tear (Selye 1946). Of course we know that stress is not necessarily destructive; Selye himself coined the term eustress to describe the positive effects of stressors that are moderate in intensity and duration. As Frederick Douglass, one of the foremost abolitionists, stated, If there is no struggle, there is not progress (Douglass 1997). The zoo community, having for the past couple of centuries given little creative attention to
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the many problems that elephants face in captivity, entered Selyes first alarm stage only recently, when the difficult issues being discussed in this conference first arose, primarily in the public forum. That initial state of alarm has hardened into a resistance to suggestions for change originating outside the zoo industry (sadly, we might argue that it is the elephant captives who are presently trapped in the third and most dangerous stage of exhaustion and decline). However, if we subscribe to Douglasss quote above, there is still hope; the organizers of this Symposium believe strongly that humans work best face to face, where they can discuss problems in a context that offers the prospect of mutual respect, the chance to be heard and a commitment to listen as constructively as possible. As a result, despite some regrettable absences, a usefully diverse group of participants from the United States, Canada, United Kingdom, Norway and Australia, concerned with research on elephants in the wild and in captivity, achieved the goals stated above, and, as the conference proceeded, demonstrated a growing willingness to approach the issues constructively. The intended beneficiaries of the dialogue were several. Elephants, of course, were primary, but so were all people concerned with them. Those in charge of the day-to-day handling of elephants in captive environments, and the managers of captive elephant programs, may benefit as much as any from constructive exchanges, for they deserve the best scientifically literate and ethically informed suggestions for going forward. There are others who will benefit ultimately from constructive debate, rigorous science and deep care about elephants. They include the informed public concerned with elephants well-being. But even greater beneficiaries may be those who wished to attend the conference but were denied approval to do so by their employers, as well as scientists and leaders of organizations who were suspicious of such a gathering and so did not attend. All these people need a voice in discussions about humanitys future with elephants. Certainly, promoting productive exchange on controversial topics with a group that includes field, academic and zoo scientists, zoo directors and former directors, sanctuary directors and welfare advocates, will be no simple task for the reasons mentioned. Everyone in this controversy is distressed: the elephants; the scientists and clinicians who study them in the wild and in captivity; those groups that are critical of the manner in which elephants are managed now and that have a different vision for the future; groups and individuals that are using novel approaches to all aspects of the captive environment and husbandry; and the people who manage elephants in traditional confined environments. However, the Tufts Symposium worked because the participants demonstrated clearly that good discussion requires willingness to examine ones own beliefs critically, and to consider dispassionately what is happening to elephants, what is happening to the people handling elephants, and what may work for decision-makers controlling the fate of individual elephants now and in the future. The goal in exchanges about elephants is, of course, the deepest possible understanding of what is happening to them; those already in captivity as well as their free-living conspecifics. This goal will be achieved soonest through a convergence of insights about how to marshal resources and solve problems, and consensus on how to move forward in ways that benefit these animals we all hold in such regard. It can be enlightening to consider what might motivate anyone to undertake a careful examination of the well-being of elephants confined to built environments. For some, the scientific method is enoughwhat can we perceive is really happening with the captives? Is their health good or bad? What happens to a large-brained, intelligent animal when it is removed from its natural social milieu and kept in an enclosure a millionth or less the size of its potential range in the wild? For some, interest in these elephants is stimulated by any apparent distress. Among others who
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observe elephants in captivity, elephants extraordinary abilities and their differing personalities are what provoke interest. Scientists can easily understand this, but they also know that sometimes humans do not see the worlds varied realities well, or at all, especially when what they study is nonhuman realities. The Symposium brought together experts on free-ranging elephant populations and on elephants under close human management. Our goal was to describe and discussin a setting conducive to open exchangesthe tools and limits of science necessary to assess elephant well-being. Accordingly, we believe that this book serves as a necessary foundation for future development of innovative, rational and ethical strategies of stewardship. An elephant in the room We began with the wellspring of information on which we hope to build the future of elephants in captivity: the science of their behavior in the wild. In Section One, Wild Ethology, Poole and Granli, Lee and Moss, and Williams discuss a variety of factors pertaining to elephants core interests. The description of the biophysical, ecological and social life of wild elephants rests on the foundation of allometry, the science of size, which has been described by William Calder III, a foremost theoretician in the field, as the most significant (and predictive) biological characteristic of an animal (Calder III 1984). Section Two, Health, Psychological Trauma and Stress: Effects on Welfare contains chapters by Bradshaw, Kaufman and Martin, and Mikota. Harkening back to Selyes description of the third stage of the adaptation syndrome, these authors address the effects of trauma, and the contrasts between freedom and captivity, on the health and well-being of creatures held captive. Bradshaw and Mikota in particular draw their arguments from comparisons of the effects of captivity and distress on humans and elephants. Kane and Stroud both ponder Current Management Assumptions in Section Three. They take a close look at the belief systems underlying many of the traditions that still prevail in the practice of keeping elephants in captivity, and discuss potential sources of these long-held beliefs. In Section Four The Science of Captive Elephant Welfare, first Barber, then Maple, Bloomsmith and Martin, and finally Mason and Veasey, while acknowledging that lack of information is not a license for neglect and abuse, focus on the scientific assessment of welfare among confined elephants, pointing out that defining welfare is the first and, surprisingly, most difficult problem and that, while many questions pertaining to elephant welfare may appear to have obvious and intuitive answers, intuition is not invariably supported by scientific results. These authors argue that Best Practices cannot yet be developed because so many questions remain to be validated by empirical research. Section Five, Science-Based Management, addresses practical methods used to alter two fundamental aspects of the lives of most elephant captives: lack of exercise, and free contact management, or any management system based on negative reinforcement and punishment. Kinzley presents techniques to increase captives species-typical behaviors, while Whittaker and Laule describe how application of learning principles enhances autonomy and protects staff by focusing on positive reinforcement and physical separation of animals and caregivers. In Section Six on Novel Strategies, Buckley, Derby and Sheldrick help us make the transition from ameliorations of traditional practices to implementation of completely different approaches that are used now only for traumatized wild elephant infants and elephants in captivity that are declared surplus and are often ill. These are the orphanages and sanctuaries that are still regarded with skepticism by many professionals (but see Williamson, Chapter 18).
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In the final section of the book, Hancocks and Williamson present their New Visions, models that might transform current management of elephants in urban settingsand beyond. Waldau then offers a vision for going forward in the afterword, Celebrating Our Future with Elephants. Practical, theoretical and ethical importance of meaningful guidelines for elephants in captivity Today we face particularly serious questions. Are we, the very species responsible for the endangered status of elephants in the wild, capable of providing these same creatures a benign form of captivity? And must we wait for the knowledge only available through empirical science to develop best practices to govern such captivity? Answers to these questions will shape our future way of coexistingour modus vivendi with these particularly marvelous, enigmatic and interesting nonhumans. We know that elephants have unique needs: the chapters herein testify clearly to that, if it is not always obvious how to measure those needs. We editors trust that, because of changing attitudes towards animal welfare, fewer people now are sufficiently unfeeling to deny that, in past forms of captivity, the accommodation of elephants needs was a miserable failure. We also believe that present forms of captivity are too often inadequate. The Symposium was one effort to identify and develop respectful ways to share information and find ways to solve recognized problems. We know difficulties will persist, even in simply providing optimal circumstances for captives. All individuals who are interested in animal welfare generally, and in the welfare of elephants in captivity specifically, will need courage and political will to face the toughest issue of all: whether any form in which elephants are held in captivity can meet their real needs. If a majority believes the answer to that proposition is No, then those individuals who are involved with the management of confined elephants, and with the conservation and management of elephants in the wild, must be prepared to hear how and why such a conclusion was reached. For these and other reasons, guidelines must be examined regularly. When science shows that existing guidelines are inadequate, a frank and ethical response is required, with a renewed commitment to better alternatives. If humans choose to hold and care for elephants, then a combination of scientific knowledge and ethical responsibilities is required for best management. In many ways, each of the essays in this book exhibits this essential combination, even when authors are consciously (and rightly) committed to a scientific focus. The guidelines set forth in Appendix II are a joint effort of the Coalition for Captive Elephant Well-Being (CCEW) that grew out of a white paper by Kane, Forthman and Hancocks (Appendix I), and reflect a synthesis of science and ethics. For example, they insist on the provision of environments that address the spectrum of species-specific behaviors. Further, the guidelines concerns for individuals, for the importance of the elephants perspective, and for training based upon positive reinforcement, reflect both good science and the bedrock ethical concern to do no harm. The Coalitions Best Practices (Appendix II) recognize that minimal empirical research has been conducted on elephants welfare and behavioral issues in captivity. When reviewing the professional literature relevant to developing a set of Best Practices, the Coalition faced the ironic situation that the zoo industry, while insisting on best practices supported by empirical evidence, was the very industry that had historically failed to conduct such research on welfare and behavioral issues. The Coalition, therefore, turned to the extensive scientific literature on the effects of stress and
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distress on laboratory animals. Reliance on metrics derived from such studies by drawing conservative inferences is well accepted in the scientific community. It is, for example, the foundation of animal trials of medicines intended for human use. The application of the paradigm of laboratory test results to elephants in captivity in North America is particularly pragmatic. If for no other reason than their size and relative scarcity, elephants are not well suited to any traditional form of empirical research. Further, the American zoo industry houses elephants in very small groups scattered across the continent in an archipelago of sites, all operated independently of the others. This peculiar dispersion of animals and loci of authority over them has, so far, stymied independent and empirically rigorous research on the animals welfare. This does not mean, however, that good science on issues central to elephants well-being does not exist. Scientists and nonscientists alike have been astonished by the stunning discoveries of the natural sciences in the last two centuries; discoveries that have threatened to topple ancient world views and inaccurate explanations of the physical world. Careful science, based on relevant laboratory studies and scientifically rigorous, longitudinal studies of elephants in the wild, is the foundation of a high standard of elephant welfare. Careful science also contributes greatly to our ability to map the world as we perceive itand is pertinent to what ought to be happening now to elephants in present forms of captivity. The editors believe that humans, especially those in Western society, are at a turning point. Science cannot solve all problems, but it can help us learn ways in which to move forward. In this sense, the issues discussed in the Symposium, and the ideas presented in this book and translated into potential actions in the Coalitions Best Practices, are a preeminent exercise in the use of science to see the possibilities of a more compassionate and complete relationship with elephants. Several American zoos have given up their elephant programs in recent years: Chehaw Wild Animal Park in Georgia, Chicagos Lincoln Park Zoo, the Frank Buck Zoo and the Gladys Porter Zoo in Texas, Henry Vilas Zoo in Wisconsin, the Louisiana Purchase Gardens and Zoo, Mesker Park Zoo, Indiana, the Alaska Zoo, the zoos in Detroit, Philadelphia, Sacramento and San Francisco, and Lion Country Safari in Florida. Zoos phasing out elephant exhibits include the Bronx, Santa Barbara, and Buttonwood Park in Maine. This book is notably offered, however, to those zoos choosing to stay the course with elephants. We believe that the following chapters demonstrate amply that the challenges of exhibiting and maintaining elephants in captivity in a manner that is both ethical and scientifically defensible are as massive and complex as the animals themselves. We fervently hope that all individuals who are in any way responsible for elephants in captivity will use this book to help them with thoughtful and sincere attention to a too-long neglected problem: an elephant in the room that now demands open debate.

References

Abram D. 1996. The spell of the sensuous: perception and language in a more-than-human world. New York, NY: Pantheon Books. Calder WA III. 1984. Size, function and life history. Cambridge, MA: Harvard University Press. Douglass F. 1997. Narrative of the life of Fredrick Douglass. New York, NY: New American Library. Selye H. 1946. The general adaptation syndrome and the diseases of adaptation.J Clinic Endocrinol 6:117-230. Retrieved December 3, 2007 from http://www.garfield.library.upenn.edu/classics1977/ A1977DM03500001.pdf. xvii

Introduction
Debra L. Forthman From Aristotle to Audubon, there have always been naturalists out in the world carefully observing and describing animals. They have illustrated, counted, tracked and collected: netting, trapping and shooting animals for close study, and banding and marking them for growth measurements and to monitor behavior. In so doing, they have greatly enriched our knowledge of the natural world. But their observations of nature, although often affectionate, only illuminated a limited distance, focused as they were on populations or species. Though Aristotle noted no animal has, at the same time, both tusks and horns, he did not describe particular examples of tusked and horned species and, while Audubon never for a day gave up listening to the songs of our birds, or watching their peculiar habits, or delineating them, he did not establish a relationship with them as individualsespecially not the one hundred or so he shot daily for his paintings. Even Konrad Lorenz, a founder of the field of ethology, did not give names to the individual Greylag geese imprinted on him, though they followed at his heels as if he were their mother. Only within the past 40-50 years has the study of animals involved the patient collection of detailed information over time about individuals living within the context of varied social organizations. This individualization of animal behavior has caused a revolution in our understanding of personalities like Echo the elephant and Flo the chimpanzee, and a realization that terms like personality, cognition and culture may be applied as equally to elephants and chimpanzees as to human beings. Poole and Granli describe carefully and eloquently in our opening chapter how evolution has shaped elephants to be what and who they areunique creatures that nonetheless possess hallmarks previously thought of as the sole provenance of humans. Using data from the same population, Lee and Moss detail vital elements in the life cycle of elephants, as well as sex differences in life trajectories; they use both to compare average life-spans in a free-living versus a captive elephant population. Finally, Williams offers data relevant to the management of wild Asian elephants. He focuses on sex differences in ranging and habitat use, underscoring the prevalence of fragmented habitats, some degraded by human abuse, some by the elephants themselves while confined in areas bisected by impassable human structures (e.g. dams). To my mind, this section, which offers contrasts and, sometimes, comparisons between the life and well-being of wild individuals and those in captivity, is essential in informing all that follows.

References

Wikipedia, retrieved September 5, 2007, http://en.wikipedia.org/wiki/Aristotle#Biology_and_medicine. Wikipedia, retrieved September 5, 2007, http://en.wikipedia.org/wiki/John_James_Audubon and http://www.brainyquote.com/quotes/authors/j/john_james_audubon.html. 1

Chapter 1 Mind and Movement: Meeting the Interests of Elephants


Joyce Poole and Petter Granli Amboseli Trust for Elephants and ElephantVoices The Elephantidae, once widespread across the continents of America, Europe, Asia and Africa, now occur as fragmented remnants in parts of Asia and sub-Saharan Africa (Meredith 2001). Three species, African savanna and forest elephants (Loxodonta africana and Loxodonta cyclotis) and Asian elephants (Elephas maximus) represent the impoverished remains of what was once a rich family tree. The elephants have evolved over 50 million years from small creatures (Shoshani & Tassy 1996) to increasingly large-bodied, long-lived animals dependent upon moving over vast distances in search of food, water, minerals and social and reproductive partners (e.g., ATE database; Lindeque & Lindeque 1991; Verlinden & Gavor 1998; Whyte 2001). Physically impressive and vigorous, an adult male African elephant may be four meters tall and weigh as much as 7,000 kg. No other terrestrial animal alive today weighs even half as much (Haynes 1991). With a maximum lifespan in the wild of over 65 years (Moss 2001), the extant elephants are unusually long-lived mammals (Eisenberg 1981). Excluding mortality caused by humans, the life expectancy of a freeranging female elephant is 54 years (ATE database), an age not very different from our own species in the absence of medical care. Elephants in zoos and circuses are plagued by a host of physical and psychological ailments (Clubb & Mason 2002; Schmidt 2002; Kane, Forthman & Hancocks, Appendix I) that are not observed among their free-living counterparts. Regardless of the regular health care they receive, and despite the lack of human predation and the vagaries of drought and disease, captive elephants suffer from obesity, arthritis, foot problems and reproductive and psychological disordersand die at a younger age (Clubb & Mason 2002; Lee & Moss, Chapter 2). Unlike free-living elephants, those kept in zoos show relatively low fertility and a high rate of stillbirths; they also encounter difficulties giving birth and raising their young (Clubb & Mason 2002). Furthermore, they may engage in a wide variety of abnormal behaviors such as stereotypic swaying, killing of infants and hyper-aggression toward other elephants. What are the underlying causes of these abnormal physical and psychological disorders? A look at some of the essential elements of the lives of free-ranging elephants provides some compelling answers. In the wild, elephants are rarely still; some segment of their bodies, whether legs, ears, eyes, trunk or tail, is in motion. Despite their great size, elephants are vigorous animals, perpetually active in mind and body. Apart from the two to three hours of a 24-hour day when wild elephants may stand or lie down to sleep, they are searching over vast areas for food, water, companions and mates or they are actively engaged in preparing a food item for ingestion, interacting with a conspecific or another species or occupied in some frivolity. Their movements may be deceptively
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slow, allometrically befitting of such an enormous animal, but even when their bodies are at rest, their minds are active. Elephants are large-brained, intelligent and inquisitive animals (Rensch 1956, 1957; Shoshani & Eisenberg 1992; Poole 1998; Roth 1999; Cozzi, Spagnoli & Bruno 2001; Hart, Hart, McCoy & Sarath 2001; Hakeem, Hof, Sherwood, Switzer et al. 2005; Douglas-Hamilton, Bhalla, Wittemyer & Vollrath 2006; Plotnik, de Waal & Reiss 2006; Shoshani, Kupsky & Marchant 2006; Poole & Moss 2008); we only need watch the tip of an elephants trunk, the posture of its ears and the angle of its head to gain a window into its actively engaged mind. In the wild, everything elephants do is an intellectual challenge: locating and manipulating a wide variety of food items; remembering the location of water during a drought; searching for potential mates; deciding where to go, who to go with, who to join and who to avoid. Discriminating between the individual scents, voices and appearances of hundreds of familiar and unfamiliar individuals, including friends and foes, relatives and non-relatives, higher-ranking and lower-ranking competitors and friendly and unfriendly other species is a continually engaging activity. What happens to the psychological and physical well-being of such intelligent creatures when we remove the need to search for or manipulate widely dispersed and diverse food items? Or when we eliminate the multifaceted demands of being part of a large social network in a complex and fluid society? The stated aim of zoos is to meet the behavioral and biological needs of the species they hold captive. When it comes to elephants, however, zoos are woefully inadequate. Zoo proponents and welfare activists alike have tended to focus on the proximate causes of suffering in captive elephants (e.g., foot problems, arthritis, reproductive health issues, obesity, hyper-aggression, stereotypic behavior). But unless we address the ultimate source of captive elephant sufferingthe overall lack of biologically relevant mental stimulation and physical activitywe will never meet their behavioral and biological needs. We must ask ourselves whether meeting their requirements is an attainable goal, and, if so, within what constraints. The perspective that we take in this chapter is that an elephant-centric approach is possible, though certainly expensive and challenging. Nonetheless, we choose to believe that discerning future zoo visitors will demand to experience thriving elephants if they accept them in captivity at all. On the move Free-living elephants are on the move at least 20 out of every 24 hours (Figure 1), actively engaged in foraging, exploring, socializing and searching for conspecifics. Activity patterns of wild elephants vary enormously depending upon the season, and the age, sex, reproductive state and population of an individual (ATE database). In Amboseli, elephants spend between 30 and 55 percent of daylight hours feeding (low end of the range: lone musth males; high end of the range: non-musth males), five to 15 percent walking while feeding (low: male elephants in bull groups; high: elephants in mixed groups), 15 to 55 percent walking (low: non-musth sexually inactive males; high: males in musth), three to 23 percent interacting (low: non-musth sexually inactive males; high: musth males), three to 15 percent resting (low: musth males; high: sexually inactive non-musth males), and approximately five percent collectively engaged in standing, comfort activities and drinking. While adults usually rest standing during the day, they frequently sleep lying down for a couple of hours at night. Modern elephants exist across a broad range of habitat types from deserts to swamps, lowland rainforests, gallery and montane forests, upland moors, floodplains, open savannas and woodland. Ranging from sea level to as high as 4,875 meters (Grimshaw, Cordeiro & Foley 1995), elephants
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Chapter 1 - Mind and Movement: Meeting the Interests of Elephants

Figure 1. Elephants follow a daily routine in Amboseli: walking from the bush lands across the open plains to the swamp. (Photo: Petter Granli)

can survive extreme temperatures for short periods, yet they thrive between 15 and 35 degrees Celsius, typically seeking shade or water above 30 degrees Celsius. In rare cases, elephants have become adapted to desert conditions, for example in Gourma, Mali and Kaokoveld and Damaraland in Namibia (Leggett 2004). Across these habitats the home ranges of individual male and family groups vary tremendously from 15 to approximately 11,000 km2. Very few studies report home ranges of less than 100 km2 and these probably represent incomplete datasets. In Kruger National Park, South Africa, for example, the ranges of adult females vary in size from 86 to 2,776 km2, with a mean of 880 km2 (Whyte 2001). In Northern Botswana, home range size averages over 1,000 km2, varying from 447-3,309 km2 with some groups traveling up to 200 km in search of dry-season water (Verlinden & Gavor 1998). In the semi-arid savanna of the Samburu-Laikipia region of Kenya, elephant ranges vary from 102-5,527 km2 (Thouless 1996), while in the more arid environments of Namibia, ranges may vary from 2,136-10,738 km2, with a mean of 5,860 km2 (Lindeque & Lindeque 1991). Asian elephants, a typically forest-dwelling species, and African forest elephants generally have smaller home ranges than African savanna elephants. The home ranges of Asian elephants fluctuate between 34 and 800 km2 for females, and 200 and 235 km2 for males, though some home ranges appear to cover thousands of square kilometers (Sukumar 2003). Elephants living in harsh desert conditions characteristically have the largest home ranges. In the best-studied desert population in northwest Namibia, elephants survive seasonally scarce water and forage by moving over vast areas of up to 12,600 km2 (Viljoen 1987, 1989; Viljoen & Bothma 1990; Lindeque & Lindeque 1991; Leggett, Fennessy & Schneider 2003; Leggett 2005). The variation in home range can, to a large extent, be explained by habitat type, though home range also varies considerably within populations, and individual preference, tradition, interfamily relationships, sex and season all play a role in determining home range size (ATE database). Despite the fact that the elephants energetic cost of walking is the lowest recorded for any living land animal (per gram of tissue one-fortieth the rate of a mouse; Langman, Roberts, Black, Maloiy et al. 1995), elephants still behave in ways to conserve energy (Wall, Douglas-Hamilton & Vollrath 2006). Consequently, smaller home ranges generally reflect higher habitat quality and vice versa. Proponents of the modern zoo have used this fundamental energetic truth to argue that since elephants in captivity are provided with food and water they do not require large spaces. For instance, Bill Foster, past President of the American Zoo and Aquarium Association (AZA), was
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reported by the Deseret Morning News (2005) as saying that the reason animals move so much in the wild is to seek security or food, but in zoos with food, protected environments and veterinary care, elephants live enriched lives. Yes, they can move miles, he said, but only because they have to. Nothing could be further from the truth. Over millions of years, as large-bodied animals, the elephants have evolved a range of specialized physical and behavioral adaptations to allow them to cover long distances so as to meet their ecological, social and reproductive requirements. In other words, elephants are adapted for long-distance living, just as polar bears are adapted for arctic climates. To survive long walks without access to water, elephants have developed a pharyngeal pouch for water storage. To defend themselves and their offspring from large carnivores and human hunters, elephants evolved a tightknit, highly cooperative society, and elaborate parental care and defense behaviors. To adapt to a life where those close companions and potential mates may be separated by many kilometers, elephants have evolved a range of specialized traits allowing them to produce, receive and localize distant, very low-frequency acoustic and seismic signals (Heffner & Heffner 1982; Fischer 1990; Nummela 1995; OConnell, Hart & Arnason 1998; Reuter, Nummela & Hemila 1998; Weissengruber, Egger, Hutchinson, Groenewald et al. 2006a). Unique and morphologically peculiar, the relatively inflexible, pillar-like legs and cushioned feet of elephants have evolved to support their vast weight (Weissengruber & Forstenpointner 2004) and enable them to walk efficiently over long distances on rough surfaces. The skeletons of the mammoths, mastodonts and modern elephants are all similarly inflexible, characterized by columnar legs and a nearly horizontal spine, which offer support for their heavy bodies, and lacking flexed joints. Unlike those of other animals, the upper and lower portions of the legs are aligned almost vertically when the limbs are extended (Haynes 1991), and the maximum forward and rearward motion of the legs is limited so that the legs are almost always beneath the body. The design of the muscular structures, too, matches the precise requirements of heavy weight-bearing, as well as of Proboscidean limb posture and locomotion patterns. For example, the musculoskeletal foot arch is designed in a manner that allows an elephant to stand on an extensive cushion such that none of its toes touch the ground. Each toe has separate muscles, indicating that movements of the digits, such as spreading and contracting, are important. The toes of the elephant are then embedded within a common skin-shoe. Both the musculoskeletal foot arch and its cushioning provide an important shock-absorbing function. The proper posture of the foot and its skeletal elements likely play a key role in supporting the elephants enormous body weight and in distributing the mass over the entire sole (Csuti, Sargent & Bechert 2001); elasticity mechanisms aid in minimizing stress and energy consumption during both resting and locomotion (Weissengruber & Forstenpointner 2004). Some of the features described above, which make elephants so well-designed for living in large spaces, become the very reasons for their unsuitability in the traditional zoo. For example, individuals so behaviorally and emotionally well-adapted to living in a close-knit society must often live in captivity without companions. A species so beautifully designed for the detection of meaningful (e.g., conspecifics, thunder) low-frequency sound (Heffner & Heffner 1982; Poole, Payne, Langbauer & Moss 1988) and seismic vibrations (OConnell, Hart & Arnason 1998; Reuter, Nummela & Hemila 1998), is exposed in city environments to continuous low-frequency machine, vehicle and air traffic noise, which may interfere with inter-individual communication and likely influences negatively both their psychological and physiological health (Rylander 2004). Endowed with a high concentration of Vater-Pacinian corpuscles (sensitive to pressure and vibration) in the cushions of the feet and Meissner corpuscles (mechanoreceptors) in the adjacent skin,
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the elephants foot is highly sensitive (Weissengruber et al. 2006a). The elephants large body and rather inflexible limb joints, so well adapted for energy-efficient locomotion, are particularly vulnerable to arthritis in a sedentary captive environment (Weissengruber, Fuss, Egger, Stanek et al. 2006b). The pads of an elephants foot are designed for walking long distances on uneven and rough surfaces, not for standing on concrete. As a result of the predominantly stationary existence on smooth surfaces, the feet of captive elephants wear unevenly (Schmidt 2002), causing improper posture of the feet, and consequently of the legs and spine, leading to painful arthritis and other joint problems (Figure 2). G. Weissengruber (pers. comm. March 31, 2006) found in zoo elephants that not only the joints of the extremities but also the joints of the vertebral column were affected by pathologic alterations. The uneven wear shows up regularly in zoos (Schmidt 2002). The adage use it or lose it applies aptly to captive elephants: Elephants need to walk to stay well. Walking to stay well applies to more than just an elephants physical health. Elephants in small spaces with little mental and physical stimulation also exhibit stereotypic behavior, rocking and swaying. In an elegant comparison across carnivores, Clubb and Mason (2003) showed that species that were naturally wide-ranging were more vulnerable to welfare problems in captivity, including psychological dysfunction and stress as exemplified by stereotypy. Proponents of the modern zoo have claimed that data from the wild is not necessarily applicable to zoo elephants. For example, Hutchins (2006) claims that data from the wild show elephants to be extremely flexible animals. Though his observation is correct, no zoos come close to meeting the lower range of environmental or social parameters that exist in nature. If the general state of

Figure 2. Asian female, Toni, crippled by arthritis; photographed at the National Zoo in 2005. (Photo: Petter Granli) 6

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elephants in captivity were one of thriving, this might be acceptable, but it is not (e.g., Clubb & Mason 2002). Other zoo managers (e.g., Stephen Thompson, Director of Conservation at Lincoln Park Zoo, quoted in Kennedy 2005) go further, asserting that research from the wild is not applicable to zoo elephants because captive elephants have different requirements from free-ranging elephants. The argument may have its roots in the long-term tradition of keeping captive elephants and in a misunderstanding of the term domesticated. In biological terms, domestication refers to changes in the genetic makeup of a population that affect the physical or behavioral character of individuals, a process which is likely to take hundreds generations of selective breeding. Elephant capture and taming began in the Indus Valley around 4,000 years ago and Asian elephants have continued to be captured, trained and worked since that time. Asian elephants are often referred to as a domesticated species, but this is an erroneous use of the term. The vast majority of captive elephants in each generation have been wild-caught, and among the minority born in captivity, most are probably the progeny of wild fathers. In addition, there has been no selection to create domestic breeds among Asian elephants. The number of generations of captive-bred elephants is not sufficient for any physical or behavioral adaptations to occur and therefore it is incorrect to refer to or think of them as a domesticated species. So, while elephants may become habituated to, or tamed by, human beings, they are still wild animals with the same inherent physical, behavioral, social and emotional interests as wild elephants. The interests of captive elephants anywhere should clearly be based on conclusions from studies of elephants in their natural habitat. Mental and physical challenges in the daily life of a wild elephant The activities experienced by a free-ranging elephant motivate an active mind and keep fit a vigorous body. No matter what the arenaforaging, defending, socializing or reproducingan elephants daily life is distinguished by need, purpose, challenge, choice, will, autonomy and camaraderie. Social learning, too, is seen in many aspects of an elephants daily life and is a vital component of mental activity. These elements, so fundamental to the lives of wild elephants, are currently all but absent in captivity. Foraging Elephants continue to grow throughout most of their lives due to delayed epiphyseal fusion of the long bones (Haynes 1991). Owing to their enormous size, indeterminate growth, long and energetically expensive reproductive lives and lack of a specialized digestive system, elephants must consume vast quantities of food, and foraging occupies the majority of an elephants daily movements. Each day an adult eats 150 to 450 kg, or four to six percent of its body weight, and drinks 100-160 liters of water. To realize this input, elephants must spend almost three-quarters of a 24-hour day foraging (Wyatt & Eltringham 1974; Lindsay 1994). Effective foraging is achieved through constant smaller and larger movements: the coordinated action of feet, tusks and dexterous trunk selects individual items of fruit, tugs up tufts of grass, opens heart of palm, flattens the hard thorns of an acacia branch or strips bark off trees; slow meandering carries an elephant from one food item to another; purposeful walking takes an elephant through a variety of habitats on a daily basis and migrations on a seasonal basis. The physical activity and mental stimulation involved in the search for food items (walking, reaching and smelling with the trunk), their manipulation (digging, kicking, stabilizing with the feet; prying, levering and breaking with the tusks; pulling, ripping, breaking, defoliating, cleaning with the trunk), their ingestion (trunk and tongue) and mastication constitutes the very core of an
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elephants interest and survival. Many of the techniques used by wild elephants to locate, select and extract food must be learned, either through experience or by watching others, and social learning plays a critical role in calves acquisition of foraging knowledge and techniques of manipulating food items (Lee & Moss 1999; Figure 3). The lack of space available in zoos and circuses does not permit elephants to search for, select from, learn about and manipulate a wide variety of food items, thus depriving elephants of much-needed physical activity and mental stimulation. A few zoos have introduced food spreads (Kinzley 2006; Chapter 12) and while these are a breakthrough in elephant husbandry, it is a timeconsuming and expensive process requiring dedicated staff. A complex network of relationships in time and space Wild elephants live in a complex fission-fusion society that is remarkable for its fluidity on the one hand, and its close and enduring social relationships on the other. Elephant relationships radiate out from the mother-offspring bond through family, bond group, clan, sub-population, independent adult males and even beyond the population to strangers (Moss 1988; Payne 2003; Poole & Moss 2008). Within this social arena, the lives of adult female and male elephants differ radically (Poole 1994). An intricate network of bonds among individuals and families typifies the lives of females and their offspring, while fluctuating sexual states distinguish the dynamic activities, associations and relationships of adult males (Moss & Poole 1983; see Boxes 1 & 2; Figure 4). The social relationships of elephants are particularly complex because individuals interact with many animals from different social units across a population, and cooperative social partners may not always be together in the same group. Members of the same family are frequently kilometers apart, and much of a familys daily activity may be focused on approaching close associates or circumventing individuals they wish to avoid. This pattern of attraction and evasion is clearly illustrated by the patterns of simultaneously radio-tracked individuals (Charif, Ramey, Langbauer,

Figure 3. Elephant calves learn what to eat by sampling food items from the mouths of their relatives. (Photo: Petter Granli)

Joyce Poole & Petter Granli

Figure 4. An intricate network of bonds between individuals and families typifies the lives of females and their offspring. (Photo: Petter Granli)

Box 1. Families and Bond Groups The close and lasting social relationships formed by female elephants are remarkable in the context of their fluid social system (Archie et al. 2006). Elephant families are composed of a discrete, predictable composition of (mostly) related individuals, but over the course of hours or days, these groups may temporarily separate and reunite, or they may mingle with other social groups to form larger social units or aggregations. Such groupings may be predicted on close social and genetic bonds, home range and season (Douglas-Hamilton 1972; Moss & Poole 1983; Sukumar 2003; Wittemyer, Douglas-Hamilton & Getz 2005; Archie et al. 2006; Moss & Lee in press). Habitat type, season, relatedness, personality traits, tradition, deaths of influential members and the strength of a matriarchs leadership all play a role in the cohesiveness of families (Moss and Lee in press). In general, elephant families are smaller in forest habitats and larger in mixed savanna habitats (Sukumar 2003). Over years, families may split to form bond groups (Douglas-Hamilton 1972; Moss and Poole 1983; Wittemyer, Douglas-Hamilton & Getz 2005) or, sometimes, fuse to form new families (Moss & Lee in press; ATE database). Close acquaintances may be distinguished by association patterns, greeting behavior, coordinated movement and decision-making, and strong affiliative, cooperative and defensive behavior (DouglasHamilton 1972; Dublin 1983; Moss & Poole 1983; Lee 1987; Moss 1988; Poole 1998; Payne 2003). Individuals who have no close relatives within their family still benefit from the same cooperative behavior (Archie et al. 2006).

Chapter 1 - Mind and Movement: Meeting the Interests of Elephants

Box 2. Male Society


The social life of a wild male elephant is mentally and physically challenging. Developing in the tightly bonded society of females, young males maintain close relationships with their relatives and participate in social events affecting their family, albeit at lower intensities than their female age-mates (Lee and Moss 1999; Lee, Poole & Moss in press). By age nine males begin to spend time away from their families, and by 14 they have usually departed (Lee & Moss 1999). Newly independent males must acquire fresh skills to adapt to the society of males where body size and fluctuating sexual state determine interactions and relationships (Poole 1989a). During the transition, young males social activities center on getting to know age-mates, and playing with novel partners from outside the natal family (Lee 1986; Lee et al. in press). In this way males gather information crucial to longevity and reproductive success (Poole 1989a, 1989b; Poole, Lee & Moss in press; Lee, Poole & Moss in press). Among sexually inactive adults, relationships are courteous, while interactions between those who are sexually active, particularly between those in the heightened sexual period of musth, become combative and highly aggressive (Poole 1987, 1989a). Male reproductive success is strongly dependent upon longevity; older, larger males in musth are dominant and produce significantly more offspring (Poole 1989a & b; Hollister-Smith, Poole, Archie, Vance et al. in press). The peak breeding age is between 45-50 years old. To survive to an age when a male can breed successfully requires utilizing skills that he has learned and honed over decades. A male must learn to recognize a large number of individual males by their scent, appearance and voice; remember their strengths relative to his own; keep track of which individuals are in musth, where they are located and what condition they are in; and monitor the changing location of pre-estrus and estrus females.

Payne et al. 2005; Douglas-Hamilton, Krink & Volrath 2006). The combination of social qualities observed in elephantsclose and lasting cooperative social relationships, and fission-fusion socialityexists in only a small number of cooperatively hunting carnivores (e.g., hyenas, lions and sperm whales) and a few primates (e.g., chimpanzees and humans: Archie, Moss & Alberts 2006). The social complexity hypothesis posits that intelligence has evolved to allow individuals to cope with the changing and often difficult-to-predict behavior of partners with whom they must cooperate and compete. And, like other species that live in fission-fusion societies (e.g., human beings, chimpanzees, social carnivores, whales), elephants are recognized for their intelligence and reasoning abilities (Poole & Moss 2008). Although the Amboseli elephant population is relatively small (numbering 1,500 at the end of 2006), compared to many elephant populations, it is, nevertheless, a big society. A female elephant in Amboseli may seek the company of and/or purposefully avoid literally hundreds of other individuals in the course of her daily range (Poole & Moss 2008; see Lee & Moss, Figure 7, Chapter 2). Searching from group to group for receptive females, sexually active males may also interact with
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hundreds of different individuals, both male and female, in the course of a 24-hour day (Poole & Moss 1989). The sheer number of elephants involved in an individuals social network, and the hierarchical character of the formation and dissolution of aggregations make elephants remarkable. The ability of elephants to distinguish genuine strangers from a wide range of more regular associates through recognition of voices (McComb, Moss, Durant, Sayialel & Baker 2000) and scents (Rasmussen & Krishnamurthy 2000) may be explained by the extremely large and convoluted temporal lobes of the elephants brain (Shoshani 1998; Shoshani et al. 2006). Learning from others Social learning and behavioral innovation are essential elements of individual development and of the very fabric of elephant society, tradition and culture (Lee & Moss 1999; Poole & Moss 2008). For example, social learning via allomothering (care of calves by juvenile females) provides young females with an array of caretaking experiences and skills that persist through the birth of their own first calf. This transfer of social knowledge is vital for successful mothering (Lee 1987; Lee & Moss 1999). Distinguishing between friends and foes, learning where to go to find water during droughts and where to find particular food items or minerals, is passed on from mother to daughter (e.g., McComb, Moss, Durant, Sayialel et al. 2001; Payne 2003). The acquisition of appropriate estrous and consort behavior, too, requires a social context for learning (Poole & Moss 2008). Both the acquisition of estrous behaviors and the choice of mates appear to be facilitated by the presence and behavior of the mothers of these young females (Poole & Moss 2008). The birth of a females first calf is another life event where the presence and behavior of experienced females aids inexperienced mothers. Experienced family members assist young females to cope with the physical demands of birth, including helping a newborn to its feet, and with the immediate protection and socialization of the newborn calf (Moss 1988; Lee & Moss 1999). Interaction with other elephants and the transmission of social and ecological knowledge is key to an elephants survival, and the stimulation such relations provide is, we believe, necessary for an elephant to thrive. The traditional zoo does not offer the space necessary to allow elephants to live in natural family groups, nor does it present elephants with the option of choosing associates from among other families, clans or populations or provide the opportunity for learning survival skills through experience or from others. By depriving elephants of adequate space, zoos not only severely restrict an elephants ability to obtain adequate and essential exercise, but they take away an enormous source of mental stimulation needed for the basic well-being of such a highly social and intelligent individual. The search for mates Reproductive behavior is an essential component of the daily life of any animal. In elephants, reproduction involves highly energetic physical and mental activities. Intricate chemical and acoustic signals and a finely honed memory are employed in the search over extensive areas for both rivals and mates (Poole 1989a; Poole & Moss 1989; Poole 1999). Courtship, mating, male-male competition and female choice constitute intensely interactive behavior, alternatively highly subtle and immensely overstated. The confined spaces that zoos and circuses offer do not allow for the fluid intermingling of numerous males with females and thus have a major influence on the purpose, choice, autonomy and will of an elephant. By age 30, most males have experienced their first heightened period of sexual and aggressive activity, or musth (Poole & Moss 1981; Hall-Martin & Van der Wilt 1984). Characterized by a distinct, rigid, head-high posture, swollen and secreting temporal glands, dribbling of strong-smelling
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Chapter 1 - Mind and Movement: Meeting the Interests of Elephants

Figure 5. Two males in musth battle for supremacy; fluctuating sexual states distinguish the dynamic activities, associations and relationships of adult males. (Photo: Joyce Poole)

urine (Poole & Moss 1981; Poole 1987) and distinctive vocalizations (Poole 1987, 1999; Poole et al. 1988), musth males experience impressive surges of circulating testosterone (Hall-Martin & Van der Walt 1984; Poole, Kasman, Ramsay & Lasley 1984). With the onset of musth, a males behavior goes through a striking psychological transformation. A male in musth spends the majority of his time interacting aggressively with other large adult males or enthusiastically searching for receptive females, attempting to gain access to, or guard those in peak estrus (Moss 1983, Poole 1987, 1989a, b; Poole & Moss 1989; Fig. 5). Highly active, a male in musth may pursue another male or search for a mate over many kilometers in the space of a few hours. Musth has a pivotal effect on the relative dominance ranks of males (Poole 1989a); with few exceptions, musth males, whether large or small, rank above non-musth males. The duration of musth is age-related and may also be influenced through suppression by proximity to higher-ranking males (Poole 1989a). In populations without older individuals (Slotow, van Dyke, Poole, Page et al. 2000), or in captive situations (Jainudeen, McKay & Eisenberg 1972), musth starts at a younger age and lasts longer. Like young females, young male elephants also benefit from social learning and are often observed to follow older musth males, testing the identical urine spots and the same females as the older do (Poole & Moss 2008). Musth males are extremely tolerant of these youngsters, allowing them to stand less than a meter from an estrous female, while they ensure older males are kept at long distances (Poole 1982). Successful mounting and intromission require considerable skill and practice, which may, in part, be gained by watching the behavior of older, more experienced males. Experience from southern Africa also highlights the importance of social learning in the acquisition of appropriate male reproductive behavior (Slotow et al. 2000). Juvenile male elephants who witnessed their families killed in a culling operation and then were translocated to areas without adult males, exhibited abnormal reproductive behavior as young adults, including the mounting, tusking and killing of black rhinos. While trauma is likely to have been a causal factor in the development of this abnormal behavior (Bradshaw, Schore, Brown, Poole & Moss 2005), it is also likely that
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the absence of adult male role models contributed to the inappropriate sexual reaction of these young males. The behavior ceased after the later introduction of older males (Slotow et al. 2000). Communication The fluid nature of elephant society, in which closely bonded individuals may be many kilometers apart, requires that elephants possess a communication system combining multifaceted short- and long-distance signaling. A combination of trunk, ear, limb and body postures and movements signal a broad range of agonistic, defensive and affiliative gestures and complex emotional responses (Kahl & Armstrong 2000; Poole & Granli 2003; Poole & Granli 2004). Chemical signals including saliva, mucus secretions from the eyes, fluids from the ano-genital tracts, temporal glands, ears and interdigital glands, also play an essential role in elephant social and reproductive communication (Rasmussen, Hall-Martin & Hess 1996; Rasmussen & Schmidt 1998; Rasmussen & Krishnamurthy 2000; Rasmussen & Wittemyer 2002). Elephant acoustic communication includes a broad variety of sounds with components ranging from five Hz to over 9,000 Hz (Poole in press). Calls include very low-frequency rumbles and higher-frequency trumpets, snorts, screams, barks, roars, cries, chirps, croaking and other idiosyncratic sounds (African: Berg 1983; Poole et al. 1988; Poole 1994; Langbauer 2000; Leong, Ortolani, Burks, Mellen et al. 2003; Soltis, Leong & Savage 2005a, b; Poole in press; Asian: McKay 1973). Elephants use these acoustic signals to communicate agonistic, defensive, affiliative, protective, reproductive, logistical and social messages (Poole in press). Elephants utilize powerful, very low-frequency sounds to coordinate their movements (Payne, Langbauer & Thomas 1986; Poole et al. 1988; Langbauer, Payne, Charif, Rapaport et al. 1991; Garstang, Larom, Raspet & Lindeque 1995; Larom, Garstang, Payne, Raspet et al. 1997; McComb et al. 2000). Via such acoustic signals, elephants can recognize the individual voices of other elephants at distances of up to 1.5 kilometers (McComb, Reby, Baker, Moss et al. 2002) and may detect the location of conspecifics over an area of up to 300 km2 depending upon atmospheric conditions (Larom et al. 1997). When an elephant vocalizes with a low-frequency rumble, an exact replica of this signal propagates separately through the ground. Elephants respond appropriately to this signal component (OConnell et al. 1998; OConnell-Rodwell, Wood, Rodwell et al. 2006). Elephants are capable of vocal production learning (imitation), and this rare talent may have evolved to facilitate social bonding and cohesion in the elephants highly dynamic fission-fusion society (Poole, Tyack, Stoeger-Horwath & Watwood 2005). Social learning, so fundamental to the development of elephants, plays a further role in acoustic acquisition (Wemmer & Mishra 1982; Wemmer, Mishra & Dinerstein 1985). The very rich communication system that we observe in the extant elephants is likely to have coevolved with increasing sociality and brain size (e.g., Shoshani et al. 2006). The versatile and intricate, short- and long-distance communication of elephants is yet one more indicator of their adaptation to a rich social environment and for complex use of space. Conclusion Elephants are intelligent and vigorous creatures that have evolved in expansive and complex physical and social environments. Adapted to large space, the continual search for food, water, companions and mates involves constant large- and small-scale movements that, we believe, are essential for the well-being of elephants. Based on decades of research, it is our considered opinion that todays zoos and circuses do not come close to meeting the interests of either male or female elephants. Nor do we believe that the slightly expanded exhibits that many zoos are currently contemplating, at great expense, will make a significant difference.
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Chapter 1 - Mind and Movement: Meeting the Interests of Elephants

Figure 6. Wild elephants live in a complex fission-fusion society that is remarkable for its fluidity on the one hand, and its close and enduring social relationships on the other. (Photo: Petter Granli)

It is our opinion that the interests of elephants in captivity can only be met within environments that: Enable the development of normal social relationships, the formation of families (with calves), the possibility for at least small-scale fission-fusion sociality, cooperative behavior, social learning and play; Enable choice of association and interactions among numerous social partners and mates; Enable natural foraging behavior and activity patterns; Necessitate roaming in search of varied food, social partners and mates; Inspire physical and mental activity in all aspects of daily life. Throughout this essay we have emphasized that space is crucial to the well-being of elephants; to meet each of the above criteria space is a necessity. And, by attaining these criteria, zoos will also meet a final requirement: Ensure freedom from chronic illnesses and mental and physical suffering due to lack of physical movement and mental stimulation. However, defining the minimum space needed to meet the interests of elephants is exceedingly difficult. Our belief is that two to three family groups (or 20-30 individuals) are necessary to enable the development of fission-fusion characteristics. In addition to this number, the population should include adult males. To reduce the problems of prolonged musth, a natural hierarchy should be permitted to establish, and males must have a mechanism for safe retreat. We estimate that a minimum of four to five adult males ranging in age from young adult (15-20 years) to fully mature adult (40-50+ years) should be included. To accommodate a population of 25-35 or more individuals and allow natural foraging and socializing behavior we believe 50-70 km2 (~two km2/
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individual) of varied terrain and habitat is an indication of the space required. Assuming such a scenario is acceptable, a few of these large elephant zoos could be located in the warmer climatic zones of the United States and Europe. The elephant populations in these zoos would be composed from existing zoo or circus elephants, as the capture and import of elephants from range states are unacceptable. Once a population is established, the transfer of females and calves to other facilities would be highly undesirable due to the potential trauma inflicted by the disruption of close social bonds. Rooted in our knowledge of elephant social behavior is our firm belief that it is not possible to meet fully the well-being of female elephants without the presence of calves. Yet we have strong misgivings concerning ethical issues surrounding the captive breeding of elephants and its longerterm consequences. Any such large facility holding a naturally functioning elephant population, complete with natural breeding and mortality, is likely to experience increasing numbers and, due to the confined nature of the exhibit, would have to intervene to maintain an appropriate population size. The culling of elephants has generally been extremely controversial (e.g., Owen-Smith, Kerley, Page, Slotow et al. 2006). Culling elephants in the United States or Europe would be ethically unacceptable, as would the transfer of individuals (particularly females and calves) from one facility to another. Fertility regulation, though possible, would likely lead to extremely low birth rates, since mortality in these facilities is expected to be low. The issue of captive breeding is so problematic that most elephant welfare proponents argue for no breeding whatsoever. Clearly a no-breeding policy would translate into the eventual extinction of captive elephants outside their native range. Whether this is a good or a bad thing depends upon whom you listen to, and is not within the scope of this essay to consider. We conclude merely by posing the following questions: Do we have the right to preside over the suffering of intelligent animals for our own entertainment and pleasure, whether or not they represent ambassadors for their free-living cousins? How much mental and physical suffering by individual elephants is tolerable in exchange for a measure of conservation support generated? And, is the keeping of several hundred elephants in shamefully confined spaces an acceptable way to educate the public and prevent the extinction of free-ranging elephants? Acknowledgments We thank the Office of the President of Kenya for permission to work in Amboseli National Park, the Kenya Wildlife Service for local sponsorship and the Amboseli Trust for Elephants for decades of invaluable scientific teamwork and logistical support. Attendance at the conference and this writing was made possible by support from the Amboseli Trust for Elephants, the RSPCA and the Phoenix Zoo. We thank our Amboseli Trust for Elephants colleagues and Lisa Kane and Debra Forthman for comments on the manuscript. We are grateful to the Tufts University Cummings School of Veterinary Medicines Center for Animals and Public Policy and the Coalition for Captive Elephant Well-Being for hosting the meeting upon which this volume is based, and to the Symposium Sponsors (Royal Society for the Prevention of Cruelty to Animals, Gary Fink, Phoenix Zoo, American Society for the Prevention of Cruelty to Animals, North Carolina Zoo and Oakland Zoo). Special thanks go to Paul Waldau, Lisa Kane and Debra Forthman for their organization.

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References

ATE database: Data extracted from the long-term sightings, censuses or field notes of the Amboseli Trust for Elephants, 1972-ongoing. Archie EA, Moss CJ, Alberts SC. 2006. The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants. Proc Roy Soc Brit 1-10(273):513-522. Berg J. 1983. Vocalizations and associated behaviours of the African elephant (Loxodonta africana) in captivity. Z Tierpsychol 63:63-79. Bradshaw GA, Schore AN, Brown JL, Poole JH, Moss CJ. 2005. Elephant breakdown. Social trauma: early trauma and social disruption can affect the physiology, behaviour and culture of animals and humans over generations. Nature 433:807. Charif R, Ramey R, Langbauer Jr. WR, Payne K, Brown L. 2005. Spatial relationships and matrilineal kinship in African savanna elephants (Loxodonta africana) clans. Behav Ecol & Sociobiol 57:327-338. Clubb R, Mason G. 2002. A review of the welfare of zoo elephants in Europe. Horsham, UK: RSPCA. Clubb R, Mason G. 2003. Captivity effects on wide-ranging carnivores. Nature 425:473-474. Cozzi B, Spagnoli S, Bruno L. 2001. An overview of the central nervous system of the elephant through a critical appraisal of the literature published in the XIX and XX centuries. Brain Res Bull 54:219-227. Csuti B, Sargent EL, Bechert US, eds. 2001. The elephants foot. Ames, IA: Iowa State University Press. Douglas-Hamilton I. 1972. On the ecology and behaviour of the African elephant. Ph.D. Thesis. University of Oxford, Oxford, UK. Douglas-Hamilton I. 1998. Tracking elephants using GPS technology. Pachyderm 25:81-92. Douglas-Hamilton I, Krink T, Volrath F. 2005. Movements and corridors of African elephants in relation to protected areas. Naturwissenschaften 92:158-163. Douglas-Hamilton I, Bhalla S, Wittemyer G, Vollrath F. 2006. Behavioral reactions of elephants towards a dying and deceased matriarch. Appl Anim Behav Sci 100:87-102. Dublin HT. 1983. Cooperation and reproductive competition among female African elephants. In: Wasser S, ed. Social behavior of female vertebrates. New York, NY: Academic Press. p. 291-313. Eisenberg JF. 1981. The mammalian radiations: an analysis of trends in evolution, adaptation and behavior. Chicago, IL: University of Chicago Press. Fischer MS. 1990. The unique ear of elephants and manatees (Mammalia): a phylogenetic paradox. C R Acad Sci Ser III: Sci de le vie 311(4):157-162. Garstang M, Larom D, Raspet R, Lindeque M. 1995. Atmospheric controls on elephant communication. J Exp Biol 198:939-951. Grimshaw JM, Cordeiro NJ, Foley CAH. 1995. The mammals of Kilimanjaro. J of E Afr Nat Hist 84:105139. Hakeem AY, Hof PR, Sherwood CC, Switzer RC III, Rasmussen LEL, Allman JM. 2005. Brain of the African elephant (Loxodonta africana): neuroanatomy from magnetic resonance images. The Anatom Rec Part A 287A:1117-1127. Hall-Martin AJ, Van der Walt LA. 1984. Plasma testosterone levels in relation to musth in the male African elephant. Koedoe 27:147-149. Hart BL, Hart LA, McCoy M, Sarath CR. 2001. Cognitive behaviour in Asian elephants: use and modification of branches for fly switching. Anim Behav 62:839-847. Haynes G. 1991. Mammoths, mastodonts and elephants: biology, behavior, and the fossil record. Cambridge: Cambridge University Press. Heffner R, Heffner H. 1982. Hearing in the elephant (Elephas maximus): absolute sensitivity, frequency discrimination and sound localization. J Comp & Physiol Psychol 96:926-944. Hollister-Smith JA, Poole JH, Archie EA, Vance EA, Georgiadis NJ, Moss CJ, Alberts SC. 2007. Age, musth and paternity success in wild male African elephants (Loxodonta africana). Anim Behav 74:287-296. Hutchins M. 2006. Variation in nature: its implications for zoo elephant management. Zoo Biol 25:161171. 16

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Jainudeen MR, McKay GM, Eisenberg JF. 1972. Observations on musth in the domesticated Asiatic elephant. Mammalia 36:247-261. Kahl MP, Armstrong BD. 2000. Visual and tactile displays in African elephants, Loxodonta africana: a progress report (1991-1997). Elephant 2(4):19-21. Kane L, Forthman D, Hancocks D. 2005. Optimal conditions for captive elephants: a report by the Coalition for Captive Elephant Well-Being. Retrieved 2007, from http://www.elephantcare.org/protodoc_files/ new%2006/CCEWBOptimalConditionspdf.2.pdf. Kennedy K. 2005. Chicago not for elephants, scientists tells alderman. Retrived 26 August 2005. http:// www.chicagotribune.com/news/local/chicago/chi-0505260256aug26.16522490.story?coll=chinewslocalchicago-hed. Kinzley C. 2006. Right here, right now: the Oakland zoo improves the lives of their elephants. TheCommuniqu, Feb. Silver Spring, MD: AZA. p. 15-18. Langbauer Jr. WR, Payne KB, Charif RA, Rapaport L, Osborn F. 1991. African elephants respond to distant playbacks of low-frequency conspecific calls. J Exp Biol 157:35-46. Langbauer Jr. WR. 2000. Elephant Communication. Zoo Biol 19:425-445. Langman VA, Roberts TJ, Black J, Maloiy GM, Heglund NC, Webers JM, Kram R, Taylor CR. 1995. Moving cheaply: energetics of walking in the African elephants. J Exp Biol 198(3):629-632. Larom D, Garstang M, Payne K, Raspet R, Lindeque M. 1997. The influence of surface atmospheric conditions on the range and area reached by animal vocalizations. J. Exp Biol 200:421-431. Lee PC. 1986. Early social development among African elephant calves. Nat Geo Res 2:388-401. Lee PC. 1987. Allomothering among African elephants. Anim Behav 35:278-291. Lee PC, Moss CJ. 1999. The social context for learning and behavioural development among wild African elephants. In: Box HO, Gibson KR, eds. Mammalian social learning. Cambridge: Cambridge University Press. p. 102-125. Lee PC, Poole JH, Moss CJ. In press. Male elephant social dynamics: independence and beyond. In: Moss CJ, Croze HJ, eds. The Amboseli elephants: a long-term perspective on a long-lived mammal. Chicago, IL: University of Chicago Press. Leggett KEA. 2004. Coprophagy and unusual thermoregulatory behaviour in desert-dwelling elephants of north-western Namibia. Pachyderm 36:113-115. Leggett KEA. 2005. Home range and seasonal movement of elephants in the Kunene Region, Northwest Namibia. J of Afr Zool 41:17-36. Leggett KEA, Fennessy J, Schneider S. 2003. Seasonal distributions and social dynamics of elephants in the Hoanib river catchment, northwestern Namibia. J of Afr Zool 38(2):305-316. Leong KM, Ortolani A, Burks KD, Mellen JD, Savage A.2003.Quantifying acoustic and temporal characteristics of vocalizations for a group of captive African elephants (Loxodonta africana).Bioacoustics 13:213-231. Lindeque M, Lindeque PM. 1991. Satellite tracking of elephants in northwestern Namibia. Afr J of Ecol 29:196-206. Lindsay K. 1994. Feeding ecology and population demography of African elephants in Amboseli, Kenya. Ph.D. Thesis. University of Cambridge, Cambridge, UK. McComb K, Moss C, Sayialel S, Baker L. 2000. Unusually extensive networks of vocal recognition in African elephants. Anim Behav 59:1103-1109. McComb K, Moss C, Durant S, Sayialel S, Baker L. 2001. Matriarchs as repositories of social knowledge. Science 292:491-494. McComb K, Reby D, Baker L, Moss C, Sayialel S. 2002. Long-distance communication of social identity in African elephants. Anim Behav 65:317-329. McKay GM. 1973. Behavior and ecology of the Asiatic elephant in Southeastern Ceylon. Smithsonian Contributions to Zoology 125:1-113. Meredith M. 2001. Africas elephants: a biography. London: Hodder and Staughton. 17

Chapter 1 - Mind and Movement: Meeting the Interests of Elephants

Moss CJ. 1983. Oestrous behaviour and female choice in the African elephant. Behav 86:167-96. Moss CJ. 1988. Elephant memories: thirteen years in the life of an elephant family. London, UK: Elm Tree Books. Moss CJ. 2001. The demography of an African elephant (Loxodonta africana) population in Amboseli, Kenya. J Zool Soc Lond 255:145-156. Moss CJ, Poole JH. 1983. Relationships and social structure in African elephants. In: Hinde RA, ed. Primate social relationships: an integrated approach. Oxford, UK: Blackwell Scientific Publications. p. 315325. Moss C, Lee PC. In press. Female elephant social dynamics: fidelity and flexibility. In: Moss CJ, Croze HJ, eds. Amboseli elephants: a long-term perspective on a long-lived mammal. Chicago, IL: University of Chicago Press. Nielson-Stowell A. 2005. Elephant exhibit earns pachyderm-size praise. Deseret Morning News, Retrieved Friday, June 17, 2005 from http://deseretnews.com/dn/view/0,1249,600142099,00.html. Nummela S. 1995. Scaling of the mammalian middle ear. Hearing Res 85:18-30. OConnell C, Hart L, Arnason BT. 1998. Comments on elephant hearing. J Acoust Soc Am 105:20512052. OConnell-Rodwell CE, Wood JD, Rodwell TC, Puria S, Partan SR, Keefe R, Shriver D, Arnason BT, Hart LA. 2006. Wild elephant (Loxodonta africana) breeding herds respond to artificially transmitted seismic stimuli. Behav Ecol & Sociobiol 59(6):842-850. Owen-Smith N, Kerley GIH, Page B, Slotow R, van Aarde RJ. 2006. A scientific perspective on the management of elephants in the Kruger National Park and elsewhere. S Afr J of Sci 102:389-394. Payne KB, Langbauer Jr. WR, Thomas EM. 1986. Infrasonic calls of the Asian elephant (Elephas maximas). Behav Ecol & Sociobiol 102:283-316. Payne K. 2003. Sources of social complexity in the three elephant species. In: de Waal FBM, Tyack PL, eds. Animal social complexity: intelligence, culture, and individualized societies. Cambridge, MA: Harvard University Press. p. 57-85. Plotnik JM, de Waal FBM, Reiss D. 2006. Self-recognition in an Asian elephant. Proc NAS USA 103:1705317057. Poole JH. 1982. Musth and male-male competition in the African elephant. Ph.D. Thesis. University of Cambridge, Cambridge, UK. Poole JH. 1987. Rutting behavior in African elephants: the phenomenon of musth. Behav 102:283-316. Poole JH. 1989a. Announcing intent: the aggressive state of musth in African elephants. Anim Behav 37:140-152. Poole JH. 1989b. Mate guarding, reproductive success and female choice in African elephants. Anim Behav 37:842-849. Poole JH. 1994. Sex differences in the behavior of African elephants. In: Short R, Balaban E, eds. The differences between the sexes. Cambridge, UK: Cambridge University Press. Poole JH. 1998. An exploration of a commonality between ourselves and elephants. Etica & Animali 9:85110. Poole JH. 1999. Signals and assessment in African elephants: evidence from playback experiments. Anim Behav 58:185-193. Poole JH. In press. The behavioral contexts of elephant vocal communication. In: Moss CJ, Croze HJ, eds. The Amboseli elephants: a long-term perspective on a long-lived mammal. Chicago, IL: University of Chicago Press. Poole JH, Moss CJ. 1981. Musth in the African elephant, Loxodonta africana. Nature 292:830-831. Poole JH, Kasman LH, Ramsay EC, Lasley BL. 1984. Musth and urinary testosterone concentrations in the African elephant, Loxodonta africana. J Reprod Fert 70:255-260. Poole JH, Payne KB, Langbauer, Jr WR, Moss CJ. 1988. The social contexts of some very low-frequency calls of African elephants. Behav Ecol & Sociobiol 22:385-392. 18

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Poole JH, Moss CJ. 1989. Elephant mate searching: group dynamics and vocal and olfactory communication. Symp Zool Soc Lond 61:111-125. Poole JH, Granli PK. 2003. Visual and tactile signals of African savanna elephants, http://www.elephantvoices. org/index.php?topic=what_comm&topic2=what_comm/visual_tactile_signals.html. Poole JH, Granli PK.2004. The visual, tactile and acoustic signals of play in African savannah elephants. In: Jayewardene J, ed.Endangered elephants, past, present and future. Proc sym on human-elephant relationships and conflicts, Sri Lanka, September 2003. Colombo: Biodiversity and Elephant Conservation Trust. p. 44-50. Poole JH, Tyack PL, Stoeger-Horwath AS, Watwood SL. 2005. Elephants are capable of vocal learning. Nature 434:455-456. Poole JH, Lee PC, Moss CJ. In press. Long-term reproductive patterns and musth. In: Moss CJ, Croze HJ, eds. The Amboseli elephants: a long-term perspective on a long-lived mammal. Chicago, IL: University of Chicago Press. Poole J, Moss C. 2008. Elephant sociality and complexity: the scientific evidence. In: Wemmer C, Christen K, eds. Never forgetting: elephants and ethics. Baltimore, MD: Johns Hopkins Press. Rasmussen LEL, Hall-Martin A, Hess DL. 1996. Chemical profiles of African bull elephants (Loxodonta africana): physiological and ecological implications. J Mammal 77:422-439. Rasmussen LEL, Schmidt BA. 1998. Chemical signals in the reproduction of Asian (Elephas maximus) and African (Loxodonta africana) elephants. Anim Reprod Sci 53:19-34. Rasmussen LEL, Krishnamurthy V. 2000. How chemical signals integrate Asian elephant society: the known and the unknown. Zoo Biol 19:405-423. Rasmussen LEL, Wittemyer G. 2002. Chemosignaling of musth by individual wild African elephants (Loxodonta africana): implications for conservation and management. Proc Roy Soc Lond 269:853860. Rensch B. 1956. Increase of learning capability with increase of brain size. Am Natur 90:81-95. Rensch B. 1957. The intelligence of elephants. Sci Am 196:44-49. Reuter T, Nummela S, Hemila S. 1998. Elephant hearing. J Acoust Soc Am 104:1122-1123. Roth, G. 1999. Kleine Gehirnegroe Gehirne. Evolutionre Aspekte und funktionelle Konsequenzen. Naturwiss. Rundschau 52:213-219. Rylander R. 2004. Physiological aspects of noise-induced stress and annoyance. J Sound & Vibra 277:471478. Schmidt M. 2002. Jumbo ghosts: the dangerous life of elephants in the zoo. Philadelphia, PA: Xlibris Corporation. Shoshani J. 1998. Understanding proboscidean evolution: a formidable task. Tree 13:480-487. Shoshani J, Dalen A, Watson G, Marchant GH, Marsac E. 1997. The pharyngeal pouch: a unique receptacle in the throat of an elephant. In: Proc of the 23rd nat conf AAZK, Inc. American Association of Zoo Keepers, Inc. p. 14-24. Shoshani J, Eisenberg J. 1992. Intelligence and survival. In: Shoshani H, ed. Elephants: majestic creatures of the wild. Singapore: Weldon Owen. Shoshani J, Kupsky WJ, Marchant GH. 2006. Elephant brain. Part I: Gross morphology, functions, comparative anatomy, and evolution. Brain Res Bull 70:124-157. Shoshani J, Tassy P. 1996. The proboscidea. New York, NY: Oxford University Press. p. 472. Slotow R, van Dyke G, Poole J, Page B, Klocke A. 2000. Older bull elephants control young males: orphaned male adolescents go on killing sprees if mature males arent around. Nature 408:425-426. Soltis J, Leong K, Savage A. 2005a. African elephant vocal communication I: antiphonal calling behaviour among affiliated females. Anim Behav 70:579-587. Soltis J, Leong K, Savage A. 2005b. African elephant vocal communication II: rumble variation reflects the individual identity and emotional state of callers. Anim Behav 70:589-599.

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Sukumar R. 2003. The living elephants: evolutionary ecology, behavior, and conservation. New York, NY: Oxford University Press. Thouless CR. 1996. Home ranges and social organization of female elephants in northern Kenya. Afr J of Ecol 34:284-297. Verlinden A, Gavor IKN. 1998. Satellite tracking of elephants in northern Botswana. Afr J of Ecol 36:105116. Viljoen PJ. 1987. Status and past and present distribution of elephants in Kaokoveld, South West Africa/ Namibia. S Afr J of Zool 22:247-257. Viljoen PJ. 1989. Spatial distribution and movements of elephants (Loxodonta africana) in the northern Namib desert region of the Kaokoveld, South West Africa/Namibia. J Zool Soc Lond 219:1-19. Viljoen P.J, Bothma J Du P. 1990. Daily movements of desert-dwelling elephants in the northern Namib desert. S Afr J of Wildl Res 20(2):69-72. Wall J, Douglas-Hamilton I, Vollrath F. 2006. Elephants avoid costly mountaineering. Current Biol 16(14):528. Weissengruber GE, Forstenpointner G. 2004. Musculature of the crus and pes of the African elephant (Loxodonta africana): insight into semiplantigrade limb architecture. Anat Embryol 208:451-461. Weissengruber GE, Fuss FK, Egger GF, Hutchinson JR, Groenewald HB, Elsasser L, Famini D, Forstenpointner G. 2006a. The structure of the cushions in the feet of African elephants (Loxodonta africana). J Anat 209:781-792. Weissengruber GE, Fuss FK, Egger G, Stanek G, Hittmair KM, Forstenpointner G. 2006. The elephant knee joint: morphological and biomechanical considerations. J Anat 208:59-72. Wemmer C, Mishra HR. 1982. Observational learning by an Asian elephant of an unusual sound production method. Mammal 46:557. Wemmer C, Mishra H, Dinerstein E. 1985. Unusual use of the trunk for sound production in a captive Asian elephant: a second case. J Bombay Nat Hist Soc 82:187. Whyte IJ. 2001. Headaches and heartachesthe elephant management dilemma. In: Schmidtz D, Willot E, eds. Environmental ethics: what really matters, what really works. New York, NY: Oxford University Press. p. 293-305. Wittemyer G, Douglas-Hamilton I, Getz WM. 2005. The socioecology of elephants: analysis of the processes creating multitiered social structures. Anim Behav 69:1357-71. Wyatt JR, Eltringham SK. 1974. The daily activity of the elephant in the Rwenzori National Park, Uganda. E Afr Wildl J 12:273-289.

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Joyce Poole is Director of ElephantVoices and is on the Scientific Advisory Committee of the Amboseli Trust for Elephants. She has studied African elephants since 1975, working primarily in Kenyas Amboseli National Park. Her research work has focused on elephant reproductive and social behavior with special emphasis on communication. Throughout her career Joyce has actively engaged in issues affecting the welfare and conservation of elephants. Petter K. Granli co-directs ElephantVoices, an elephant communication research and web-based educational project collaborating with the Amboseli Trust for Elephants. Petter has a background in management and communication. Joyce and Petter may be contacted at: Amboseli Trust for Elephants, P.O. Box 15135, Langata 00509, Nairobi, Kenya and ElephantVoices, Buskhellinga 3, 3236 Sandefjord, Norway or by email at: jpoole@ elephantvoices.org and pgranli@elephantvoices.org.

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Chapter 2 - Welfare and Well-Being of Captive Elephants

Chapter 2 Welfare and Well-Being of Captive Elephants: Perspectives from Wild Elephant Life Histories
Phyllis C. Lee1,2 and Cynthia J. Moss2 Behaviour and Evolution Research Group, Department of Psychology, University of Stirling1 and Amboseli Elephant Research Project, Amboseli Trust for Elephants2 There are a number of current debates in the zoo world focused on elephants and their well-being and welfare. One of these relates to enclosure size as discussed by Poole and Granli (Chapter 1); another to protected contactits benefits and costs (e.g., Whittaker & Laule, Chapter 13); another to social needs. Yet others emphasize illness and causes of mortality in relation to natural or expected life span (see Clubb & Mason 2002). A final issue of controversy is that of captive breeding. The social and environmental factors affecting reproduction, survival and longevity in the wild are the focus of this chapter, with the aim of contributing to the development of an understanding of these issues for captive elephants. No single factor determines well-being, and wild elephants exhibit a huge range of behaviors in response to their constantly changing social and physical environments. We aim here to present some of this range, and explore their underlying dynamics. Some in the zoo community have suggested that the environment of captive elephants is that of captivity, and thus there is little that knowledge of wild elephant behavior and life history can contribute to captive welfare (Hutchins 2006). It is also the case that relatively few studies have yet to address enrichment (environmental or behavioral) for captive elephants (Shepherdson 2003). There are few quantitative assessments of whether protected contact reduces stress and behavioral anomalies, although the qualitative evidence is compelling (see Whittaker & Laule, Chapter 13). A few studies have attempted to assess physiological markers of stress in captive elephants (Brown 2000; Stead, Meltzer & Palme 2000; Ganswindt, Heistermann, Palme, Borragan et al. 2003), but we do not yet have a sufficient baseline on the physiology of environmental or social stress to make firm conclusions about what causes stress or when it occurs. Indeed, these aspects of captive life need urgent attention and research if managers aim to provide rich and rewarding environments for existing captive elephants. Despite our lack of quantitative knowledge about the captive environment, elephant biology and behavior reflect their evolutionary ecology; therefore, what they do in the wild, how they do it, how often and why can inform us about best practices for elephants in captivity. Our goal here is to illustrate vital elements of the life cycle for wild African savanna elephants (Loxodonta africana) to provide a context for comparisons between captive and wild conditions. We also explore the differences between male and female elephants life cycles to illustrate sex differences and the complex dynamics of an elephants long life.
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We have not made ecological comparisons of the use of space by either sex, or attempted to determine space needs. Rather we have focused on those social and physical factors that underlie well-being and thus which should inform spatial requirements. Suffice it to say that wild African elephants are active for approximately 18-20 hours each day, that the movements of males and females are determined both socially and ecologically and that elephants can travel as far as 50-80 kilometers in a day in a home range as small as 10 or as large as 20,000 km2 (see Douglas-Hamilton, Krink & Vollrath 2005; Leggett 2006; Poole & Granli, Chapter 1). We suggest that it may be more important to provide enough space for individuals to have the choice to be social or solitary as well as some landscape diversity, than to provide large but unchallenging areas lacking natural forage, shade or water features. Thus, the aims of this chapter are as follows: 1) To explore the differences between elephant male and female life cycles in order to illustrate the complexity of their long life span. The reproductive histories of males and females are placed into the context of their life cycles, specifically addressing those factors affecting reproductive onset and sexual function. 2) To discuss socialization and the compelling evidence that social learning opportunities are vital to the expression of normal behavior (e.g., foraging, infant care, dominance and mating). 3) Finally, to examine longevity and survival and ask why some elephants have such long lives in the wild. It is worth emphasizing that a significant difficulty in captivewild comparisons of longevity has to do with cause of death; humans actively manage the life span of their captive elephants often for reasons unrelated to normal biology. The question for managers is why do so many captive elephants experience physical or behavioral abnormality, illness or injury to the point where euthanasia is a major cause of captive mortality, and why does this occur at a relatively young age? General methods The results we present here derive primarily from the Amboseli Elephant Research Project (AERP), and these are compared with some other wild African and Asian (Elephas maximus) elephant populations. The AERP was started by Cynthia Moss and Harvey Croze in 1972, with identification of individuals and records of basic demographic, social and ecological data. The last family was completely identified by 1982. Over 2,200 elephants have been individually recognized and the population is monitored continuously. Births and deaths, and, opportunistically, estrus, musth and copulations, have been recorded from 1972 to the present. Focal animal samples of behavior and interactions, as well as systematic scan samples of activities and associations, are used to present details of behavior. The analyses presented here are based on events up to the end of 2004 (C.J. Moss, unpublished long-term records). Age is known for individuals under the age of 35 (using known birth dates) and is estimated reliably for those born before 1972 based on shoulder height, back length, tusk eruption and growth; estimated ages are reassessed periodically by using early photographs and reference to the maturational changes among the known-aged sample. Finally, for jaws found post-mortem, estimated age was checked against tooth age (see Moss 2001). Animals with estimated ages represent only 15 percent of the current sample (346 individuals out of 2,173). Cause of death, both natural and human-related, was recorded and accuracy of knowledge about death cause and death dates was noted. Human-caused deaths have been separated in the analyses that follow (N = 348).
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Chapter 2 - Welfare and Well-Being of Captive Elephants

We have used Kaplan-Meier proportional hazards analyses, assuming that hazards ratios were not constant over time, to examine mean and quartiles of survival time for first birth, first musth and longevity, with standard error and Brookmeyer-Crowley 95 percent confidence intervals. Where covariates were explored in survival analyses, we used Cox Regression and present Wald statistics. We used logistic regression analysis to explore probability of death between groups of individuals, and the Wald statistic was used as goodness-of-fit for the model functions. Univariate ANOVA was used to explore main effects and interaction of categorical variables on continuous measures. All data were tested to ensure normal distributions, and were log-transformed for normality before using parametric tests. Non-parametric Spearman correlations were used to test relationships between two variables where a normal distribution could not be approximated. All probabilities are two-tailed and set at p<0.05 for significance. Statistical analyses were made with SPSS version 13.0. Male life cycle One of the basic characteristics of the male life cycle (Figure 1) is the very long period of social and physical maturation (Lee & Moss 1999). Dependence on the family prior to social maturity and leaving the natal family can be as long as 18 years. In populations with natural age structures, including large, old males, an additional post-independence period of another 10 to 15 years is common before a male commences reproductive musth cycles. Reproductive onset

F IR S T MUS TH
B irth-7yrs : s exually immature; with natal family; mean s urvival = 77% 8-16 yrs : s perm ons et c .10 yrs ; s perm in quantity 16+yrs ; depart family c . 8-16 yrs ; mean s urvival = 93% 17-25 yrs : interes t and as s oc iation with females ; mean s urvival = 90% 25-35 yrs : 1s t mus th c . 30 yrs ; as s oc iation w/ female groups alternating with bull groups ; mean s urvival = 81%

>35 yrs : Fully c ompetitive with other mature bulls ; more attrac tive to females ; mate guarding obs erved; mean s urvival 36-50 = 54%

S E XUAL L Y AC T IVE

10

20

30

Age Age (years)

40

50

60

70

Figure 1: Male life cycle based on 32 years of observations in Amboseli National Park, Kenya (Poole, Lee & Moss in press). Survival for each age group is based on the likelihood of surviving from age one to age two for natural mortality only. Male survival to age seven = cumulative probability of surviving to seven years for male calves. 24

Phyllis C. Lee & Cynthia J. Moss

(spermatogenesis) for males occurs around eight to 10 years of age, but at this point males are only two-thirds the size of a fully adult female, and thus might have some physical difficulty mating. By the time a male is regularly coming into musth (35+ years; Poole 1987) he is one and one-half times the size of a large adult female (Figure 2). Male African elephants exhibit indeterminate growth and increase in stature for the majority of their lives. Males grow faster than females from infancy and for longer over the life span (Figure 2), with obvious energy costs to sustaining this growth (Lee & Moss 1995). In the wild, bigger is better, with larger individuals more likely to survive and to commence reproduction earlier (Lee, Poole & Moss in progress). While there is considerable variation in final stature among individuals and across populations, the shape of the growth curve up to 15 years is consistent across a wide range of populations (Shrader et al. 2006). Growth in early life is probably an excellent indicator of the mental and physical health of individuals. In Amboseli, males leave their families at an average of about 14 years of age, with considerable individual variation (Figure 3); some will spend short periods away even as young as six years. In forest elephants (Loxodonta cyclotis), males who appear to be weaned only recently (four to six years of age) travel on their own or form groups with other bulls, both large and small (P. Lee, pers. observPetit Loango, Gabon Jan. 1997; Fishlock, pers. comm. April 2005Mbeli, Congo). At this stage we cannot yet determine what causes some males to leave their families before they are

Figure 2: Growth in stature (shoulder height) for 548 measurements on 314 males and 436 measurements on 297 female Amboseli elephants (P.C. Lee, AERP long-term records).

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Chapter 2 - Welfare and Well-Being of Captive Elephants

even half the size of a female and others to stay until they are as large as their mothers. Departure appears to be the result of a large number of factors such as maternal status, family size, male friendships with peers, relative and absolute size, confidence and other individual characteristics which interact with the local ecology and population densities. While it is not yet possible to describe rules governing male dispersal, wild males forcibly removed from a family social context and lacking experience with older males can become exceptionally aggressive to other elephants and other species (Slotow et al. 2000; Slotow & van Dyk 2001; Bradshaw et al. 2005). Male social life In Amboseli, males tend to live in areas that are ecologically distinctive, and which often are less central to female areas. Asian and African males appear to engage in risky behavior in general, wandering into areas where contact with humans is likely, crop raiding, and generally covering larger ranges, as well as encountering other males who may be competitors (Sukumar 1989; Tchamba et al. 1994; Osborn 1998). Despite the impression of lone bulls, Amboseli males are solitary for less than one-third of the time, and are typically (c. 20 percent of time, depending on age) found in small groups of two or three males (see also Evans 2006). All-bull groups can, however, be comprised of over 40 animals (J.H. Poole, AERP long-term records). Being solitary or in small groups may, again, increase males susceptibility to environmental risks or hazards from

110

100

90

80

Mean (95 CI)% Time Away

70

60

50

40

Mean (95 CI) % Time away 30


20

10 0 N = 52 5 50 6 65 7 79 8 91 9 94 10 93 11 84 12 77 13 71 14 69 15 67 16 46 17 44 18

Figure 3: The age-related patterns of departure from the family (Lee & Moss 1999; Lee, Poole & Moss in press). 26

Phyllis C. Lee & Cynthia J. Moss

humans. Newly independent males tend to spend most of their time (c. 70 percent; Lee, Poole & Moss in press) with female (non-mother) groups. Even males aged 25-50 years associate regularly with females, spending 25-50 percent of their time with these groups (Figure 4). Thus, males are not asocial; they associate regularly with female groups, form groups with other males and have consistent male associates in these groups (friends: Lee, Poole & Moss in press). Males can and do get along with other males, and are well tolerated by females. Male elephants in captivity For many social mammals with lengthy periods of development, such as primates or elephants, rearing in contexts that lack some proportion of the age-sex range typically found in social groups in the wild tends to produce individuals with inappropriately extended juvenile-type behavior. In particular, play, aggression and sexual interactions are frequent and misdirected (Slotow et al. 2000; La Prairie 2001; Slotow & van Dyk 2001; Suomi 2003). Thus it would seem reasonable to leave males with familiar or family females until the age at which they become sexually active. In the wild, females are relatively rarely aggressive towards family males before dispersal, but they do target non-natal males with escalated aggression, occasionally acting in concert with other females to poke, chase or drive away the young males. It might be suggested that some experience as the target of aggression by older animals may be vital to a males ability to learn to respond appropriately to aggressive interactions, suppressing hyperaggressive responses. In captivity, the rapid and prolonged growth of males could pose health risks. Big can become too large with attendant negative physical and physiological consequences for health. Obesity and joint and foot problems may be associated with reduced potential for movement, leading

60 50

% sightings by sex (N = 29894)

40 30 20 10

% sightings by sex (N = 29894) 0 Male S olitary Bull Group MixedGroup group Mixed Cow-calf Cow-calf group Group

Figure 4: The average grouping patterns of Amboseli elephants as a percent of sex-specific sightings (all ages of independent males combined; AERP long-term records; N = Male groups = 18,490; N= female groups = 21,716).

27

Chapter 2 - Welfare and Well-Being of Captive Elephants

to further negative consequences for health. In captive contexts males may be seen as less desirable; they are more aggressive and therefore dangerous to keepers and other elephants. Given limited space, they can be difficult to house socially with females or other males once regular musth sexual activity commences. Males have both social needs and strong sexual and competitive motivations which make keeping them in naturalistic conditions problematic unless there is sufficient space for separate areas where males can withdraw from others (bull or retirement areas: Moss & Poole 1983) as well as opportunities and space to make social contacts when individuals seek companionship. As we emphasize, social dynamics underlie spatial needs especially for adult males. Welfare considerations require that the varied social and associated spatial needs of males be met in the design of captive enclosures. Female life cycle Elephant females in the wild can have extremely long reproductive and social lives (Figure 5). Females are less prone to mortality than are male elephants (Moss 2001; see below), although the energy costs of reproduction and lactation probably contribute to some increased natural mortality risks, especially during droughts. The average female born in Amboseli can survive until her late 40s or early 50s (Moss 2001; see below) and give birth to a calf every four to five years (median interbirth interval = 50 mo, range = 22-114 mo, N = 949: Moss & Lee in press a). Over 80 percent of these calves will survive to age five, and three generations of grandmothers, mothers, daughters and granddaughters form the basis of the stable savanna elephant family (see also Archie, Moss & Alberts 2006).

B irth-8 yrs: Probability of female survival to 8 = 83%

9-20 yrs: F irst birth; IB I to 2nd calf = 57.5 mo F irst calf survival to 8 = 62% ; Mean survival = 95%

20-50 yrs: E xperienced prime mothers IB I = 50 mo C alf survival to 8 = 79% Mean survival = 70%

50-65+ yrs: Old females, declining fertility & grandmothering IB I = 54.5 months C alf survival to 8 = 57%

S E XUAL L Y AC T IVE

10

20

30

Age

40

50

60

70

Figure 5: Female life cycle based on 32 years of observations in Amboseli National Park, Kenya (Moss & Lee in press a). Survival for each age group is based on the likelihood of surviving from age one to age two for natural mortality only. Calf survival to age eight = cumulative probability of surviving to eight years for both male and female calves for each category of female by parity or age. 28

Phyllis C. Lee & Cynthia J. Moss

In Amboseli, a female first gives birth at an average of 14 years, although females as young as nine have produced calves (Figure 6). Given a 22-month gestation, these younger females experienced their first fertile estrus at around seven years of age. As the figure suggests, the clustering around 14 years is quite marked; only four percent of females give birth when younger than 11 years, and seven percent when older than 16 years. What makes a female reproductively successful? In Amboseli, as elsewhere in Africa, females tend to show considerable seasonality in their fertility patterns (Lee, Lindsay & Moss in press). Low quality diets, poor body condition and time and energy spent searching for food all appear to reduce conception probabilities, and females take about three months to regain condition and conceive after a long dry season (Foley, Papageorge & Wasser 2001; Rasmussen, Wittemyer & Douglas-Hamilton 2006). In Amboseli, first-time mothers have reduced success in rearing infants, with 33 percent of firstborn calves dying early in life (under 24 months of agethe age of nutritional dependence from the mother) compared to only 13 percent for experienced mothers (Moss & Lee in press a). In the wild, a female at 12-14 years will be only 70 percent of her full adult height and will have another 20 years of growth ahead of her at the same time that she is reproducing, suggesting additional energetic and/or metabolic costs associated with growth for these young females. Inexperience also plays a role in the poor reproductive performance of first mothers; even in the wild, with extensive practice in caring for calves as an allomother or helper, they still have difficulties with calf suckling, with learning calf signals of hunger or distress, and with ensuring that calves remain close by at all times. As mothers age and gain experience with calves, their calves have higher survival rates and mothers appear to learn to discriminate in favor of behaviorally-demanding, faster-growing sons who receive a greater allocation of milk and are weaned later (Lee & Moss 1986; Lee & Moss in press). Thus, experienced mothers of sons tend to have longer intervals (55 mo) between successive births. Another critical factor in calf survival is whether the mother has helpers. Allomothers, nulliparous females aged five to 15, contribute significantly to calf survival in Amboseli, even
Figure 6. Proportional hazards model of age at first reproduction for 326 females with known ages at first birth (see also Moss 2001); median age = 13.9 (95 percent CI = 13.6-14.2).

29

Chapter 2 - Welfare and Well-Being of Captive Elephants

when absolute family size is taken into account (Moss & Lee in press a). In the wild, a variety of predatorslions, hyenas, wild dogs and, throughout the millennia, humansprey on vulnerable young calves. At birth a wild calf will only weigh 70-150 kg (Hanks 1979), making it easy prey for large social predators. Allomothers, grandmothers and the familythe social context for calves are key to ensuring calf survival (Lee 1987; Lee & Moss in press). Along with their defensive functions, allomothers are gaining experience that can contribute to their ability to rear their own calves, although allomothering experience alone appears insufficient to ensure firstborn survival rates that are comparable to those for larger, older individuals. Female sociality Among savanna elephants, females tend to stay socially bonded and closely associated with members of their family from birth to death. These genetic and affiliative bonds are the bedrock of sociality upon which is layered a rich and dynamic domain of interactions and structures. Groups of female elephants, by contrast to family units, are fluid aggregations of individuals coming and going, including one to many adult males in almost half of occurrences (see Figure 4), where the individuals move together and apart, interact with and explore each other. Families can associate with other families in such large aggregations. In Amboseli, every family has been seen at least once with each of the other 50+ families in the population (Moss & Lee in press b). Social knowledge extends to almost all others within a population of some 1,200 individuals. There are occasions when family females are not all together in the same social group. Some members of a family will form a fragment or a sub-unit, and each fragment may associate separately with different larger groups. The fission and fusion of individuals occurs over a full 24-hour period (Figure 7). The tendency to fragment and associate with non-family groups contrasts with a tendency to remain in a single coherent and cohesive unit, either in a group with just other family members or to join with others in larger groups as an intact family. This latter inclination to group with others, to be gregarious, is also highly variable among different families. In Amboseli,
Figure 7: The group size experienced by one female, Sandy, of the SA family over a 24-hour period. The SA family consisted of 11 individuals, including four adult females (Lee and Lindsay, pers. observ. March 16-17, 1984).

30

Phyllis C. Lee & Cynthia J. Moss

cohesiveness of families ranges from 100 percent to less than 50 percent of time together. Further, the larger the family and harsher the environmental conditions, the less cohesive families become (Moss & Lee in press b). The affinity for gregariousnessbeing with other elephantsis a basic elephant need. Finding a female completely on her own, when she is not ill or in estrus, is extremely rare in Amboseli. Even female forest elephants, known for their smaller family unit and group sizes, are likely to be found with at least one and often two other elephants (Theuerkauf, Ellenberg & Guiro 2000; Morgan & Lee 2007). Asian elephants tend to form groups of six to eight individuals (Vidya & Sukumar 2005). In some habitats, even savanna elephants also have very small but nonetheless cohesive families (e.g., 4-6 individuals: Mikumi, Tanzania; Mofulu 2005). The point here is that female elephants are highly dependent on relationships with other elephants; these relationships are based on genetic kinship (Archie et al. 2006) and extensive networks of knowledge (McComb et al. 2000) and persist over a females lifespan. Relationships are fundamental to negotiating elephants complex ecological and social environments (see Archie et al. 2006) as well as their success in rearing calves as discussed above. Female elephants in captivity Keeping an elephant female in captivity is a financial, management and spatial commitment that may outlast the housing institutions future, and is certainly longer than the working life span of the average keeper. Given the importance of the family to reproduction and survival, it would seem essential to keep social units intact to act in some form as a family to ensure stable structures and reduce social stresses. Unfortunately, there appears to be relatively little debate in the zoo community about female elephants needs for social stability and continuity; they are moved about constantly (one might suggest like furniture) in the interests of institutions and exhibits, not elephants social needs. While arguments can be made about the need to manage genetic diversity, since males and females are almost never housed together for life, inbreeding seems unlikely. And, if as we argue here, females reproduce more effectively in families, then using arguments about genetic management could be in conflict with strategies for captive breeding. Can families be created? In the wild, females can be left on their own due to natural demographic processes (Moss & Lee in press b) or due to catastrophic human intervention such as in Queen Elizabeth National Park, Uganda (Nyakaana et al. 2001) or Akagera National Park, Rwanda (K. Fawcett, pers comm. Dec 2006). Under such conditions, unrelated females will form long-term cooperative bonds that act and appear structurally as families. Allowing opportunities for both contact (potentially over 24 hours) and sufficient space for individuals to choose to be apart as well as together can facilitate the formation of family-like sociality in captivity. Once established, however, the trauma of subsequent separation should be recognized and accounted for in long-term group management. It is vital to note that elephant social and environmental experiences in the wild are not confined to the hours that keepers work. One significant improvement to any management routine would be to allow social access, as well as opportunities for social escape, on a 24-hour basis. This means restructuring indoor and outdoor facilities to ensure group and individual access ad libitum with associated costs and security considerations. With regard to captive reproduction, we have noted a number of factors that affect fertility and calf survival in the wild. Fat females who exercise little, as in captivity, would not be expected to show any seasonality to conception. However, obesity and lack of exercise may result in other stressors or cause hormone imbalances that reduce estrus frequency or efficiency and thus fertility
31

Chapter 2 - Welfare and Well-Being of Captive Elephants

probabilities. Although the physiological controls on puberty are poorly understood for both wild and captive elephants, the relatively narrow age window within which we observe first reproduction in the wild might suggest why females in captivity have such difficulties conceiving when they are not given access to breeding opportunities until over the age of about 18. When institutions attempt captive breeding, we also suggest that considerable care needs to be taken to ensure that females have had some experience with calves prior to their first pregnancy. Given the relatively lower calving success of primiparous mothers compared to experienced mothers even in the wild, losses are to be expected in a captive context. Managers need to be clear about the costs and benefits of captive breeding, including calf death, poor publicity and sustained interventions for hand rearing which will perpetuate the cycles of calf mortality due to inexperience. Immature femalesthe typical and essential allomothers in the wildhave not been observed to threaten or hurt calves in Amboseli. Protective and defensive interactions on the part of allomothers are triggered by infant distress vocalizations, which cause the allomothers to crowd in near the calf and to contact the calf with their feet, trunks or body. Such contacts are clearly defensive rather than aggressive and act to ensure that the calf is on its feet, close to a protector and moving away from any potential threats. If such behavior can be anticipated, then successful allomothers could be created by allowing unrestricted access to new calves, rather than attempts to check what may appear to keepers to be overly enthusiastic interest in newborns. The social context for learning and development The social context is vital for much learning in elephants. Learning what vocalizations represent (their meanings) occurs within groups; spatial knowledgewhere resources such as water and food are located, how to move on safe and unsafe routes, where areas of risk from predators or humans existall of these require repeated exposure which occurs initially in a family and in the larger group context (Moss 1988). Interestingly, males can and do wander into unfamiliar or high-risk areas after leaving their families (Lee, Poole & Moss in press), but as we discussed above, this may contribute to their greater vulnerability to mortality risks. Elephant calves also learn about foods socially: their temporal availability, processing and handling requirements, and quality (Lee & Moss 1999). Almost all foods are first experienced in a social context, since calves begin to forage at around six months but cannot sustain themselves energetically until after two years of age. Younger calves do not have the strength or height to forage on many of the foods in the wild, and thus depend on sampling (and scrounging from) others in the form of trunk-to-mouth contacts with adults while they are feeding (Lee 1987). Sexual interactions are first observed in a group context, and their performance is practiced from infancy via mounting and chase play (Lee 1986). Knowledge of familiar individuals, of friends, enemies, competitors and of ones own size and strength are all gained through social interactions within and among families. Social experiences in the form of interactions and play have gender and age-specific patterns to their development, as in many species (Figure 8). As calves age, males in particular seek out novel partners for interactions, moving beyond the confines of their family and testing their strength and abilities with a variety of partners of different ages (Lee 1986; Lee & Moss 1999, in press). Deprive calves of social experience via play and greetings, of social novelty with partners of a variety of ages and sex, of the patterns of fission and fusion that make up a daily social experience for both males and females over the course of their development, and the likely result is an individual with deficient social, sexual or maternal skills. In effect, this produces an isolate relying on
32

Phyllis C. Lee & Cynthia J. Moss

forms of self-stimulation such as stereotypies, and unpredictable interactions with human keepers and visitors for social contact (Carstead 1996). Longevity and lifespan In the wild, maximum longevity is as yet unknown, but it is likely to be in the region of 70 years. Media reports in 2005 of a known-aged Asian zoo elephant in Thailand dying at age 86 due to tooth loss and a living Asian elephant in North America estimated to be 77 years old in 2005 (Weise & Willis 2005) make an estimate of 70 years maximum longevity reasonable for African elephants in the wild. Among African elephants, longevity is a key factor in reproductive success for both males and females (Poole 1989; Moss & Lee in press a; Poole, Lee & Moss in press). For an elephant, being old equates to being large, powerful, knowledgeable and dominant (Archie et al. 2006). However, after 50, physical aging begins to reduce fertility and paternity probabilities, and the costs of being social (group travel, food competition, interactions) have an influence on the success and status of aging elephants. One contentious issue with regard to welfare is that of longevity in captive elephants. Some analyses have suggested that mean age at death is low at about 16 years in captive European
Male Social Contacts
7 6 5 Hourly Rate 4 3 2 1 0 0-12 13-24 25-36 Age (mo) 37-48 49-60

Female Social Contacts


7 6 5 Hourly Rate 4 3 2 1 0

Figure 8. Hourly rates of aggressive contacts (poke, chase), friendly interactions (rub, greet, investigate food, invite play) and social play for male and female elephants between birth and five years old (Lee & Moss in press: N observation hours Male = 119; Female = 145)

0-12

13-24

25-36 Age (mo)

37-48

49-60

33

Chapter 2 - Welfare and Well-Being of Captive Elephants

collections (Clubb & Mason 2002), while others have found an average lifespan of 33 years for North American African elephants (Weise & Willis 2005). While Clubb and Masons (2002) analysis was only on the age for dead animals, both analyses excluded individuals that died under one year of age, which is a substantial proportion of mortality in the wild (10.5 percent of calves die < 12 mo; 13.8 percent die <24 mo), and their exclusion will obviously increase average longevity. Here, in order to present some baseline data for expectations, we present average longevity from survival analyses in the Amboseli population. As mentioned above, males and females have different survivorship probabilities and different age-specific mortality hazard rates. It is therefore necessary to consider the average longevity of sexes separately. Even when animals died under one year of age, all known live births have been included in the analyses. In Moss (2001), average longevity was given as 41 for females and 24 for males. These figures included deaths known to result from human activities (control shootings, spearings, accidents due to human agency: N = 384). When these are excluded, the Cox proportional hazards model shows that median female longevity is 54.4 years (95 percent CI = 49.5-59.3, mean = 46.7, 95 percent CI = 44.1-49.4, N = 846), that for males is 42.5 (95 percent CI = 35.3-49.8, mean = 36.4, 95 percent CI = 33.1-39.8, N = 721) (Figure 9). Using different hazards models does not change the results to any extent; the data are robust and the sample sizes large. Even with environmental
Figure 9. A) Survival probabilities for male and female Amboseli elephants excluding human-caused mortality. B) Hazard rate (smoothed lines; C.J. Moss, AERP long-term records).

1 0 .9 0 .8 0 .7

Cumulatvie survival

0 .6 F e m a le 0 .5 0 .4 M a le

0 .3 Cumulative survival 0 .2 0 .1 0 0 10 20 30 40 50 60 70 80

A g e (y e a r s )

0 .1 4

0 .1 2

0 .1

Hazard Rate

0 .0 8 F e m a le M a le 0 .0 6

Hazard Rate 0 .0 4

0 .0 2

0 0 10 20 30 40 50 60 70

A g e (y e a r s )

34

Phyllis C. Lee & Cynthia J. Moss

events that cannot occur in captivity, such as catastrophic droughts or floods, or illnesses that are treated in captivity, and including the major first year mortality, elephants in the wild or at least in Amboseli are surviving far longer than the average captive elephant. Captivity does not appear to enhance an elephants chance of survival. Managers therefore need to ask why their elephants are dying so young. Other key points are the relatively higher chances of death for males by comparison to females between birth and weaning, along with increased rates of mortality throughout life. Male mortality hazard rates increase at dispersal and again with the onset of reproductive competition, associated with their increased exposure to social and environmental risks. This sex differential in mortality in later life may not be a major problem in a captive context, but the increased vulnerability of male calves in the first several years of life should be noted. Males grow rapidly early in life and their energy intake needs are high in order to sustain this growth. If access to milk or other foods is limited, their risk of death is higher than that of female calves. They could also potentially be more physiologically vulnerable to illness due to energy imbalance and high growth rates. Conclusions If elephants are to be maintained in captivity, then a set of best, rather than minimum, practices is obviously necessary to ensure their welfare. These best practices must surely go beyond providing scatter-feeding and a 200 m2 indoor and outdoor enclosure. Allowing elephants to lie down in some 40 m2 of space may be a considerable advance in well-being over nighttime chaining, but none of these practices addresses the full range of social or physical needs of elephants as biological organisms. Defining best practices, as recently attempted by the AZA, is obviously a significant step forward in captive elephant welfare, but some form of benchmark for assessing elephant needs is urgently required, and wild behavior can at least provide key insights into these needs. If we use just a few of the traits of wild elephants that we detailed above, we can suggest that elephants are allowed free access to indoor and outdoor areas over a 24-hour period; that they be given the choice as to whether and when to associate with their social companions over this entire period; that some attempt is made to provide mixed age and sex groups, which are stable over the very long-term, all of which facilitate family-like associations in a fission-fusion social context. Loss of individuals (e.g., through mortality) is a natural feature of elephant life cycles, but this does not imply that natural loss is without consequences for the well-being of even wild animals. Family disruption and fission after loss such as that of a matriarch is common (Moss 1988; Moss & Lee in press b), and places the surviving individuals at some greater risk of mortality. Whenever individuals can be maintained socially together, this should be a priority. As we note above, elephants depend on their social companions in almost all contexts; it is vital to their welfare that managers avoid breaking up established groups. Challenging spatial environments, timetables that are somewhat unpredictable and so mimic natural foraging and group dynamics, social consistency and cohesion, and a diverse social assemblage of others bringing experiences across a range of ages, interactions, activities and contextsif these can be met in captivity, then a start towards the goal of best practices will have been made. Choice of space, choice of companions, choice of foods: what we emphasize is that priority should be given to elephant needs rather than to those driven by institutional fiscal requirements or keepers timetables. If elephant welfare conflicts with institutional priorities, then institutions need to consider whether keeping elephants in either the short- or the long-term is appropriate.

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Chapter 2 - Welfare and Well-Being of Captive Elephants

Acknowledgments We thank the Government of Kenya and the Kenya Wildlife Service for research clearance and permission to work in Amboseli National Park, and the people of Amboseli for their hospitality. S. Sayailel, N. Njiraini and K. Sayailel contributed importantly to data collection. Funding for the long-term monitoring was provided by numerous individual donors, foundations and organizations through the Amboseli Trust for Elephants and the African Wildlife Foundation over the past 34 years. Support for the initial construction of the long-term database was provided by two residential meetings at the National Centre for Ecological Analysis and Synthesis (NCEAS, NSF-UC Santa Barbara). We thank all our project colleagues, especially Harvey Croze for figures and Joyce Poole and Keith Lindsay for their comments; Tufts University Cummings School of Veterinary Medicines Center for Animals and Public Policy, and the Coalition for Captive Elephant WellBeing for hosting the meeting on which this volume is based and inviting this contribution; the Symposium sponsors (Royal Society for the Prevention of Cruelty to Animals, Gary Fink, Phoenix Zoo, American Society for the Prevention of Cruelty to Animals, North Carolina Zoo and Oakland Zoo); and Lisa Kane, Paul Waldau, and Debra Forthman for organization and feedback. References
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Lee PC, Moss CJ. 1995. Statural growth in known-age African elephants (Loxodonta africana). J Zool 236:29-41. Lee PC, Moss CJ. 1999. The social context for learning and behavioural development among wild African elephants. In: Box HO, Gibson KR, eds. Mammalian social learning. Cambridge, UK: Cambridge University Press. p. 102-125. Lee PC, Lindsay WK, Moss CJ. In press. Ecological patterns of variability in demographic rates. In: Moss CJ, Croze H, eds. The Amboseli elephant: a long-term perspective on a long-lived species. Chicago, IL: University of Chicago Press. Lee PC, Moss CJ. In press. Calf development and maternal rearing strategies. In: Moss CJ, Croze H, eds. The Amboseli elephant: a long-term perspective on a long-lived species. Chicago, IL: University of Chicago Press. Lee PC, Poole JH, Moss CJ. In press. Male social dynamics: from independence to beyond. In: Moss CJ, Croze H, eds. The Amboseli elephant: a long term perspective on a long lived species. Chicago, IL: University of Chicago Press. Lee PC, Poole JH, Moss CJ. In progress. Size matters: long-term effects of growth on African elephant (Loxodonta africana) survival and success. Leggett KEA. 2006. Home range and seasonal movement of elephants in the Kunene Region, northwestern Namibia. Afr Zool 41(1):17-36. McComb K, Moss C, Sayialel S, Baker L. 2000. Unusually extensive networks of vocal recognition in African elephants. Anim Behav 59:1103-1109. Mofulu F. 2005. The elephant population and distribution in Mikumi National Park, Tanzania. MPhil Thesis. Anglia Polytechnic University, UK. Morgan B, Lee PC. 2007. Forest elephant group composition, frugivory and coastal use in the Rserve de Faune du Petit Loango, Gabon. Afr J Ecol (online March 2007) doi: 10.1111/j.1365-2028.2007.00762.x. Moss CJ. 1988. Elephant memories. New York, NY: William Morrow. Moss CJ. 2001. The demography of an African elephant (Loxodonta africana) population in Amboseli, Kenya. J Zool 255:145-156. Moss CJ, Lee PC. In press a. Female reproductive strategies: individual life histories. In: Moss CJ, Croze H, eds. The Amboseli elephant: a long-term perspective on a long-lived species. Chicago, IL: University of Chicago Press. Moss CJ, Lee PC. In press b. Female social dynamics: fidelity and flexibility. In: Moss CJ, Croze H, eds. The Amboseli elephant: a long-term perspective on a long-lived species. Chicago, IL: University of Chicago Press. Moss CJ, Poole JH. 1983. Relationships and social structure of African elephants. In: Hinde RA, ed. Primate social relationships. Oxford, UK: Blackwells Scientific Publications. p. 314-325. Nyakaana S, Abe EL, Arctander P, Siegismund HR. 2001. DNA evidence for elephant social behavior breakdown in QueenElizabeth National Park, Uganda. Anim Conserv 4(3):231-237. Osborn FV. 1998. The ecology of crop-raiding elephants in Zimbabwe. Ph.D. Thesis. University of Cambridge, UK. Poole JH. 1987. Rutting behavior in African elephants: the phenomenon of musth. Behav 102:283-316. Poole JH. 1989. Mate guarding, reproductive success and female choice in African elephants. Anim Behav 37:842-849. Poole JH, Lee PC, Moss CJ. In press. Longevity, competition and musth: a long-term perspective on male reproductive strategies. In: Moss CJ, Croze H, eds. The Amboseli elephant: a long-term perspective on a long-lived species. Chicago, IL: University of Chicago Press. Rasmussen HB, Wittemyer G, Douglas-Hamilton I. 2006. Predicting time-specific changes in demographic processes using remote sensing data. J Appl Ecol 43:366-376. Shepherdson DJ. 2003. Environmental enrichment: past, present and future. Int Zoo Yrbk 38:118-124. Shrader AM, Ferreira SM, McElveen ME, Lee PC, Moss CJ, van Aarde RJ. 2006. Structural growth and age determination of savanna elephants. J Zool 270:40-48. 37

Slotow R, Van Dyk G, Poole J, Page B, Klocke A. 2000. Older bull elephants control young males. Nature 408:425-426. Slotow R, Van Dyk G. 2001 Role of delinquent young orphan male elephants in high mortality of white rhinoceros in Pilanesberg National Park, South Africa. Koedoe 44:85-94. Stead SK, Meltzer DG, Palme R. 2000. The measurement of glucocorticoid concentrations in the serum and faeces of captive African elephants (Loxodonta africana) after ACTH stimulation. Tydskr S Afr Vet Ver 71(3):192-196. Sukumar R. 1989. The Asian elephant: ecology and management. Cambridge, UK: Cambridge University Press. Suomi SJ. 2003. Gene-environment interactions and the neurobiology of social conflict. Ann NYAS 1008:132-139. Tchamba MN, Bauer H, Hunia A, de Langh HH, Planton H. 1994. Some observations on the movements and home range of elephants in Waza National Park, Cameroon. Mammalia 58:527-533. Theuerkauf J, Ellenberg H, Guiro Y. 2000. Group structure of forest elephants in the Bossmatie Forest Reserve, Ivory Coast. Afr J Ecol 38:262-264. Vidya TNC, Sukumar R. 2005. Social organization of the Asian elephant (Elephas maximus) in southern India inferred from microsatellite DNA. J Ethol 23:205-210. Wiese RJ, Willis K. 2005. Calculation of longevity and life expectancy in captive elephants. Zoo Biol (DOI 10.1002/zoo.20011).

Phyllis Lee has a Chair in Psychology at the University of Stirling, having been for many years a Reader at the University of Cambridge, UK. She has been carrying out field research on animal behaviour since 1975, and has been part of the Amboseli Elephant Research project since 1982. She has collaborated with a number of researchers working on forest elephants, and primates from around the world.She is the authorof one book, four edited volumes, more than 35 primary journal publications and more than 30 chapters in edited volumes. Sheworks with conservation attitudes and community conservation projects, as well as human-wildlife interactions. She may be contacted at Behaviour and Evolution Research Group, Department of Psychology, University of Stirling, Scotland FK9 4LA. Email: phyllis.lee@stir.ac.uk. Cynthia Moss has been the Director of the Amboseli Elephant Research Project, which she founded, since 1972. She gained her first elephant experience with Iain Douglas-Hamilton in 1968, and she now conducts research on the distribution, demography, population dynamics, social organization and behaviour of the Amboseli elephants. She supervises research and monitoring as well as training elephant researchers from African elephant range states. She is responsible for outreach to the Maasai community, carrying out surveys and training courses at other elephant study sites in Africa, disseminating scientific results, advocating for elephant welfare and promoting public awareness by writing popular articles and books, and making films about elephants. She was awarded a John D. & Catherine T. MacArthur Foundation Fellowship in 2002 and an honorary doctorate from Smith College, also in 2002, amongst numerous other awards and prizes for her contribution to understanding elephants. She may be contacted at Amboseli Elephant Research Project, Amboseli Trust for Elephants, P.O. Box 15135, Langata 00509, Nairobi, Kenya. Email: cmoss@elephanttrust.org.
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Chapter 3 Space Use by Asian Elephants (Elephas maximus) in Rajaji National Park, North West India: Implications for Elephants Held in Captivity
Amirtharaj Christy Williams Wildlife Institute of India of allanimals, the elephant is the most difficult for man to live with, yet its passingif this must comeseems the most tragic of allThere is mystery behind that masked grey visage, an ancient life force, delicate and mighty, awesome and enchanted, commanding the silences ordinarily reserved for mountain peaks, great fires and the sea. Peter Matthiessen Elephants are large and charismatic species that have become flagships for promoting conservation across large landscapes. It would be hard to find a better exemplar than the Asian elephant, Elephas maximus, which is instantly identified by people across the breadth and length of the Indian subcontinent either as a conservation challenge, a cultural icon or as an agricultural pest. The largest terrestrial mammal in Asia once ranged widely from the Tigris-Euphrates river system in the west, throughout Asia south of the Himalayas, and east to China (Santiapillai & Jackson 1990). Today the distribution of the Asian elephant (ca. 35,000-42,000 wild elephants) covers only a fraction of its former extensive range, and includes 13 countries from the Indian subcontinent in the west to Indo-China in the east. Asian elephants in the wild inhabit a land area of about 439,000 km2, of which only about 132,000 km2 (30 percent) are protected (Kemf & Santiapillai 2000). Also, many populations are highly fragmented and endangered and optimistic estimates indicate that only six populations of Asian elephants contain/include more than a thousand individuals in a contiguous area (Kemf & Santiapillai 2000). Even these few populations have suffered from intense poaching and thus are not thriving demographically. The size of an elephants home range gives an indication of the availability of essential resources, restrictions imposed by the size of the respective conservation area or other artificial barriers and the degree of disturbance to which the animal is exposed (Whyte 1996). Areas with plentiful food and water and minimal disturbance will have smaller home ranges. They can also be small where artificial barriers (e.g., dams, canals and habitat loss due to agricultural settlements in corridor areas) prevent elephants from using a part of their home ranges (Joshua & Johnsingh 1995). It is important from the management point of view to know which elephant groups and clans or both have been affected due to such developments, because concentrations of elephants in a restricted area could also lead to habitat degradation (Sivaganesan & Sathyanarayana 1995). In several cases ecological and administrative boundaries do not match (e.g., Joshua & Johnsingh 1995) and knowledge of elephant movements is critical for preparing management plans in such
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Chapter 3 - Space Use by Asian Elephants in Rajaji National Park, North West India

areas. In addition to crucial information about home ranges, it is also important to understand the ranging and foraging behavior and spatial use of resources within the home range. To collect data on the above-mentioned aspects, elephants in Rajaji National Park (RNP; Figure 1) have been studied intensively since December 1996 using radio telemetry. RNP, in conjunction with Corbett Tiger Reserve and the adjoining forest areas, has been designated as one of the 11 elephant reserves in India. An estimated population of 1,000 elephants is found in this tract (Singh 1995). The elephants in this area have been under assault from human disruptions, such as diversion of land for non-forestry purposes, overgrazing and excessive lopping of trees for fodder, construction of a canal and a road and rail network that has resulted in habitat fragmentation (Johnsingh, Prasad & Goyal 1990). Due to its linear shape, RNP has a long boundary, with a sizeable Gujjar (nomadic pastoralists) population inside and villages all around the periphery. The villagers main form of livelihood is agriculture. Therefore, to ensure the long-term survival of elephants, a thorough understanding of their ranging and habitat requirements is indispensable. I conducted a study on elephants and their habitats with the following objectives: 1. To describe and explain the ranging behavior of elephants in the study area; 2. To analyze seasonal use of vegetation types by elephants within the study area; and 3. To identify the major factors influencing habitat selection. Study area This study was conducted in RNP, west of the river Ganges (Figure 1). This area includes the

MA P OF R A JA JI NA T IONA L PA R K
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FR H MOHA ND FG DP FR H R HQ PHA NDOWA L A T O DE HR A DUN

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Figure 1. Map of Rajaji National Park.

H A D RI W A R FO ST RE D IS IV IO N
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Amirtharaj Christy Williams

Rajaji and Motichur sanctuaries and portions of the Shivalik and Dehradun east Forest Divisions and covers an area of approximately 600 km2. Topography in the Rajaji Sanctuary area consists of deeply dissected steep southern slopes of the Shivalik hill range, which form a series of sharp ridges, interspersed with V-shaped valleys running from northeast to southwest. The southern portion of the sanctuary is flat land constituting the northern fringe of the Gangetic plain. The altitude ranges from 400-1,000 m. There are more than 4,000 Gujjars, with about 8,300 livestock (e.g., buffalo, goats, etc.) within the study area. These Gujjars are dispersed throughout the study area in small colonies. Over 140,000 people live along the periphery of the study area; their main livelihood is agriculture. The study area is bounded by intense cultivation to the north and south and to the east it is bounded by the suburbs of the town Haridwar on the bank of the Ganges. To the west the Delhi-Dehradun highway separates the RNP from the Shivalik Forest division. Rainfall ranged from 1,300 to 1,900 mm annually during 1996-1999 with most of the rain falling during the monsoon months of July to October. However, there are brief periods of rainfall throughout the year. Three distinct seasons are recognized: winter (November to March), summer (April to June) and monsoon (July to October). Materials and methods Four male and four female elephants in RNP were immobilized with ImmobilonR (a mixture of Etorphine hydrochloride and Acepromazine; Novartis, UK) delivered with a dart gun and fitted with radio transmitters embedded on an acrylic collar (Telonics Inc., Mesa, Arizona, USA). I radio tracked three males and four females for periods ranging from one to three years. The elephants were located one to three times per week. All animals were located by homing in on the signal; a GPS was used to record a position. All the data were entered into a Lotus (IBM, Inc., USA) spread sheet. I acquired satellite images of approximately 200X200 m resolution and performed unsupervised classification, allowing the computer to identify the various land use categories (including different types of forest) based on the light reflected back by the vegetation in the forest or bare ground, as the case may be, using ERDAS IMAGINE (ESRI Inc., Redlands, California, USA) image analysis software. The initial output consisted of 10 different categories of land use as defined by their reflectance values. I then did supervised classification, indicating to the computer what land-use types were similar so that they could be combined to form one common category from the 10 different ones chosen by the computer. This was done to enable easy identification of land-use types by human eye in the field. Through this method I specified five major categories of combined land-use types. The whole study area was divided into 2X2 km grids and five random grids were chosen in each of four land-use categories that corresponded to the different vegetation type combinations within the NP. One of the land-use categories was open ground (e.g., farm lands or dry river beds). In these grids, I cut by hand a 2.8 km transect along the diagonals that had the best access. Along each transect, I measured trees in circular plots of 10 m radius every 300 m. For each tree greater than 20 cm diameter at breast height (dbh) within the circular plot, I noted the species and number of branches cut by people. I also counted the saplings (< 20-cm dbh) of the different tree species in a five-m circular plot centered within the 10-m circular plot. I then summarized the data to define the four major vegetation types plus an open-area/non-natural vegetation category. They were: Sal (Shorea robusta) vegetation; Sal mixed vegetation; Plantation; Miscellaneous vegetation type; Agriculture and open areas/degraded scrub/rau (dry river beds). The vegetation types defined here corresponded very closely with the tree species communities
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Chapter 3 - Space Use by Asian Elephants in Rajaji National Park, North West India

defined during an analysis of data collected in the study area in 1996 using similar methods (A. Christy Williams, unpubl. data). I chose to limit my analysis to these four major broad vegetation types due to the large home ranges of elephants in the study area, and to the difficulty in identifying fine differences in vegetation composition in the field. I then imported the land use/vegetation image into ARCVIEW 3.02a (ESRI Inc., Redlands, California, USA) GIS software to analyze the data on animal locations, Gujjar cattle densities and other information such as water availability. I used the ARCVIEW extension ANIMAL MOVEMENT ANALYST (Hooge & Eichenlaub 1997) to analyse the radiolocation data of the seven elephants. Animal home ranges were defined by 100 percent Minimum Convex Polygons (MCP) (Mohr 1947) and 95 percent Fixed Kernels (FK; Worton 1989) of all the locations pooled across seasons and years. MCP method was used so that comparisons could be made with elephant home ranges from other studies. To look at seasonal ranging and habitat use by individual elephants, I used 95 percent Fixed Kernels of the seasonal data. I used original Adhoc and LSCV smoothing parameters to provide a less-biased estimator than a user selected or Wortons corrections (Hooge & Eichenlaub 1997). I carried out a regression analysis of the percentage increase in home range against the number of locations to see if adequate sampling had been done to describe the seasonal range of the elephant(s). I plotted the nomadic pastoral habitations within the study area with the help of a hand held GPS (Magellan Trailblazer, Magellan Inc., San Dimas, California, USA) and counted the number of pastoralists and their livestock in each of the habitations. I plotted the data and analyzed them using ARCVIEW SPATIAL ANALYST extension, creating cattle-density maps of the study area, over which I overlaid the seasonal ranges in order to calculate the cattle densities within each elephants seasonal range. Results The four adult male and four adult female elephants were captured and collared between December 1996 and March 1998. One of the collared males was followed only for five months and hence the data were not used for analysis. The remaining seven animals were followed for periods ranging from 10 months to over three years (Table 1). As the data beyond two years did not add significantly new information to what was analyzed after two years of tracking, I chose to use only 24 months of data to describe the habitat use patterns. The number of collared males represented approximately 10 percent of the estimated male population size (Williams, Johnsingh & Krausman in press). Female elephants live in groups of related females and their associated young. Females and young associated with groups containing the collared females represented approximately 33 percent of the total estimated female and associated young population numbers (Williams et al. in press). The radio-tracked individuals ranged over an area of about 600 km2. Little dung (<1 percent) was encountered outside this area during the dung surveys, indicating that the entire elephant population (ca. 180-200) west of the river Ganges largely used this 600 km2. However, there were cases of elephant bulls and family groups straying towards Yamuna in the Shivalik Forest Division (Figure 1). On the eastern side, only a few bulls crossed over the Ganges through the Chilla-Motichur corridor. Females were not documented to cross the Rishikesh-Haridwar road.

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Amirtharaj Christy Williams

Ranging Annual and seasonal range estimates Elephants had home ranges (100 percent MCP) between 188 km2 to more than 400 km2 (Table 1). There was significant variability in the seasonal ranges across elephants, seasons and years (Table 2 and see the next paragraph). However, there seemed to be no differences between the sexes in annual home ranges. Summer ranges (95 percent FK) were the smallest of the three seasons (Table 4). Males had larger summer seasonal ranges than females (Mann-Whitney test, U = 2.0, p = 0.01). All six elephants (two males and four females) that were tracked for two annual cycles showed variability in ranging patterns between the first and second years. Summer ranges were rather small or linear in shape when compared to the ranges of the same individual or group for monsoon and winter. For example, Male T and Female A ranged more widely in the monsoon of 1998 when compared to the same season the previous year (Tables 2 & 3). The MCP estimates in Table 2 were better suited to reflect occasional wandering by the elephants than the 95 percent FK estimates in Table 3. Hence the following section refers mainly to estimates from Table 3. Males T and A came into musth in winter, while Male S came into musth in summer. All the males consistently used large ranges during their musth periods and were given to wandering widely (Table 2). Females M and D gave birth to calves in the 1997 and 1998 monsoon seasons, respectively. Their seasonal ranges in winter and summer following calving were approximately 25-50 percent of their seasonal ranges the previous year (Table 2). There was a vast difference in ranging patterns of the female M and her group between the two years that they were tracked. In the year 1998-99, she altogether abandoned the southern side of RNP and spent the entire period in the northern half before being killed in a train accident near the main road on the east. Female D exhibited similar behavior by spending most of the time in areas of fewer disturbances during winter and summer following the birth of her calf. However, her monsoon ranging pattern remained unchanged. Seasonal use of vegetation types Males avoided the use of Shorea forests during the winter and monsoon and to a large extent used the other vegetation types in proportion to their availability (Table 4). Females, on the other hand, used the mixed-plantations, miscellaneous vegetation, open degraded scrub and riverbeds (Table 4) less than expected. Females (M, D and K) who were either pregnant or had young calves at heel during the period that they were radio tracked showed either strong selection or avoidance of vegetation types (Table 6). Shorea-mixed vegetation type was either selected or used in proportion to availability by all the females (Table 4). All the elephants avoided Shorea forests during the 1997 monsoon (Table 4). The same ranging pattern was observed in the monsoon of 1998 during which all elephantsexcept females D and M, who had young calves at heellargely avoided Shorea forest. Human and cattle densities within the study area were highly correlated (Spearmans r = 0.66, p<0.0001, n = 321). Hence I used only cattle densities as an index of disturbance. Though males consistently had higher cattle densities inside their home ranges when compared to females, Female K used an area of high human and cattle density during the monsoon season; hence, including the monsoon seasonal range in calculating densities did not highlight the difference (Table 5). If the monsoon season was excluded, the mean cattle density in the home ranges of females who were pregnant or had young calves at heel (K, D and M) was much lower when compared to the males (Table 5). Female A, however, who was neither visibly pregnant nor had a young calf at heel, used
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Chapter 3 - Space Use by Asian Elephants in Rajaji National Park, North West India

Table 1. Annual home ranges (km2) of radio-tracked elephants as calculated by the minimum convex polygon method (MCP) in Rajaji National Park (1996-2001). Animal ID MaleT MaleS MaleA FemaleM FemaleA FemaleD FemaleK No. Locations 253 285 123 233 235 211 264 No. months tracked 24 24 10 21 24 24 24 Home range (MCP) 407.04 188.04 254.72 183.96 326.64 306.28 251.60

Table 2. Seasonal home ranges (km2) of elephants calculated by the minimum convex polygon method (MCP) in the various seasons in Rajaji National Park (1996-1999). Season Summer (Apr-Jun) No. locations 29 33 24 36 MCP 86.60 79.12 84.24 57.24

Year/Animal

Winter (Nov-Mar) No. MCP locations 53 51 50 32 248.92 74.56 90.28 110.40

Monsoon (Jul-Oct) No. MCP locations 39 50 40 35 45 48 29 47 55 30 38 28 31 148.52 78.64 83.32 37.12 114.36 136.96 257.84 84.12 124.28 63.12 147.40 139.36 145.60

1996-97 MaleT MaleS FemaleM FemaleA FemaleD FemaleK 1997-98 MaleT MaleS MaleA FemaleM FemaleA FemaleD FemaleK 1998-99 MaleA FemaleD FemaleK

71 72 53 64 54 67 18 42 59

307.68 53.48 46.92 65.96 208.12 129.48 192.60 52.48 152.32

32 32 50 36 30 25 37

181.00 112.44 52.32 26.00 72.76 42.84 98.24

17 22
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Amirtharaj Christy Williams

Table 3. Seasonal home ranges (km2) of elephants calculated as 95 percent fixed kernels (FK) in the various seasons in Rajaji National Park (1996-1999). Season Year/Animal Winter (Nov-Mar) No. Locations 1996-97 MaleT MaleS FemaleM FemaleA FemaleD FemaleK 1997-98 MaleT MaleS MaleA FemaleM FemaleA FemaleD FemaleK 1998-99 MaleA FemaleD FemaleK Mean SE 53 51 50 32 FK 281.04 52.360 49.00 79.360 Summer (Apr-Jun) No. Locations 29 33 24 36 FK 142.48 125.04 69.40 70.36 Monsoon (Jul-Oct) No. Locations 39 50 40 35 45 48 29 47 55 30 38 28 31 FK 71.60 108.48 48.96 53.92 181.32 30.76 405.20 144.84 146.20 69.24 180.20 175.72 67.84

71 72 53 64 54 67 18 42 59

239.84 66.16 60.16 109.12 209.28 169.00 349.68 130.00 208.92 154.15 27.05

32 32 50 36 30 25 37

181.24 190.92 72.12 23.96 80.40 83.20 53.48

17 22

33.60 33.60 94.65 15.37

129.56 27.40

areas with disturbance levels comparable to those used by males (cattle density mean = 27.7, SD = 1.5). The densities of important elephant food plants were highest in Shorea vegetation type (Table 6). Even when Shorea was excluded from the plants considered, Shorea vegetation type still had the highest densities of important elephant food plants (Table 6). This was mainly due to the contribution of Mallotus phillipensis. However, Shorea was the least used among the vegetation types (Table 4), except for females who had young calves at heel. When I looked at diversity and density of major elephant food plants in the four vegetation types, Shorea-mixed and miscellaneous vegetation type had the highest diversity of elephant food plants. Water was available everywhere during the monsoon season, so I did not consider the monsoon season when testing for differences between seasons. I could not detect a statistical difference in the distance to water between winter (Mean SE = 1311.69 83.59) and summer (Mean SE
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Chapter 3 - Space Use by Asian Elephants in Rajaji National Park, North West India

Table 4. Selection and avoidance of the vegetation associations by elephants in Rajaji National Park.
Vegetation associationa Season/Animal No. Locations Chi-Sqr Shorea Shoreamix Mixedplantations Misc. Othersb

Males 1996-97 Winter MaleT MaleS 1997-98 Winter MaleT MaleS 1997 Summer MaleT MaleS 1998 Summer MaleT MaleS MaleA 1997 Monsoon MaleT MaleS 1998 Monsoon MaleT MaleS MaleA Females 1996-97 Winter FemaleM FemaleA 1997-98 Winter FemaleM FemaleA FemaleD FemaleK 1998-99 Winter FemaleD FemaleK 1997 Summer FemaleM FemaleA 1998 Summer FemaleM FemaleA FemaleD FemaleK 1999 Summer FemaleD FemaleK 1997 Monsoon FemaleM FemaleA FemaleD FemaleK 1998 Monsoon FemaleM FemaleA FemaleD FemaleK

53 51 71 72 29 33 32 32 50 39 50 29 47 55 50 32 53 64 54 67 42 59 24 36 36 30 25 37 17 22 40 35 45 35 30 38 28 31

13.10 16.42 19.17 26.25 10.94 8.93 7.73 8.620 11.62 44.54 9.75 18.02 10.27 6.16 5.62 6.65 41.29 11.76 17.19 7.41 46.60 9.78 20.62 0.81 12.82 4.82 20.48 17.68 30.94 10.25 18.64 22.48 8.97 22.48 32.83 7.50 14.44 9.42

A A A A A S

A A A N

S A

A A

S S

A A A

A A

A A A

A A A S A 46 A A A

Amirtharaj Christy Williams

Table 5. The cattle densities (no./km2) in the seasonal home ranges of male and female elephants in Rajaji National Park (1996-99). Cattle densities With monsoon season Without monsoon season Sex Mean (n) SE Mean SE 29.70 (15) 1.72 26.59 (10) 1.26 Male Female 23.71 (24) 2.94 15.88 (12)1 0.79 Mann-Whitney U 72 2 P 0.0018 0.0001 1 Densities calculated for females K, D & M, who were either pregnant or had calves at heel Table 6. The densities (no./ha) of important elephant forage trees in the four vegetationtypes in Rajaji National Park. Forage tree density Vegetation type Shorea Shorea-mix Mix-plantations Miscellaneous With Shorea robusta (Mean) SE 578.31 40.45 277.41 24.32 162.21 20.45 86.15 14.63 Without Shorea robusta (Mean) SE 298.84 21.36 251.30 25.66 156.78 20.11 74.51 13.22

= 1299 41.48) seasons pooled across animals (t = 0.13, df = 17, p = 0.89) and years. Discussion Ranging and habitat use by elephants have been studied before in both African and Asian elephant populations (e.g., Douglas-Hamilton 1972; McKay 1973; Baskaran, Balasubramanian, Swaminathan & Desai 1995; De Villiers & Kok 1997). This is the first study in Asia where the proportion of elephants, for whom ranges have been described, has been reported (see results). From this study, I have an accurate and descriptive measure of the ranging patterns of adult males and female groups in RNP. Most of the elephant ranging seems to be confined to the National Park boundaries to the west of the Ganges, unlike on the other side, where Joshua and Johnsingh (1995) found that 40-60 percent of two elephants home ranges were outside the RNP area boundary. There seem to be very few groups using the Shivalik Forest division. However, as the elephant densities inside the Park increase, more and more elephants will start using areas outside such as the Shivalik and Dehradun Forest Divisions. The population seems to be a closed one. I could find evidence for only about three bulls crossing over the Ganges from Motichur to the Chilla side of RNP. Elephant home ranges recorded so far vary widely depending on the elephant population and the ecological conditions under which they were studied. The results from this and earlier studies (e.g., Joshua & Johnsingh 1995) indicate that adult male home ranges in RNP vary widely, ranging from about 160 km2 to over 400 km2. An earlier study on the Chilla side of RNP concluded that
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Chapter 3 - Space Use by Asian Elephants in Rajaji National Park, North West India

the small home range recorded (approx. 39 km2) for a single adult female was due to her home range being lost to developmental activity (Joshua & Johnsingh 1995). This seems to be supported by the results of our study, where the smallest female home range was about 200 km2. Most studies on African elephants have showed a strong relationship between rainfall and home range size. Home ranges of elephants in areas of higher rainfall (Tsavo west: 750 km2) were smaller than the ranges of elephants in areas of low rainfall (Tsavo east: 1,600 km2). Thouless (1996) showed similar results from his study in northern Kenya, where the home ranges varied between 102 km2 (high rainfall area) to 5,527 km2 (low rainfall area). However, human disturbance also played a significant role in influencing the range sizes. The home ranges of two adult females tracked in northern Cameroon were 3,066 km2 and 2,484 km2 respectively (Tchamba, Bauer & De Jongh 1995) and it is thought that the intensity of elephant-human conflict forced the two elephants to migrate long distances, resulting in large home ranges. De Villiers and Kok (1997) estimated, after six years of radio tracking in two nature reserves adjacent to Kruger NP, that female home ranges varied between 115 km2 and 342 km2, whereas male home ranges were between 150 km2 and 342 km2. They showed that availability of water played a significant role in the size of the elephant home ranges in the two reserves. In Asia, however, home range sizes reported (males: 160-400 km2; females: 40650 km2) are much lower due to the elephants living mainly in forested habitats with higher rainfall than recorded across many of the African study sites (Baskaran et al. 1995; Joshua & Johnsingh 1995). Individual home ranges also overlapped considerably within and between sexes in the study area as noticed in other elephant studies elsewhere (Leuthold 1977; Sukumar 1991; Jachmann 1992; Baskaran 1995; Joshua & Johnsingh 1995; Thouless 1995). However, De Villiers and Kok (1997) found that females tend to avoid each other inside their core areas (defined as 10.1 percent of their home range) and explained this as a mechanism under which high densities of elephants are able to tolerate each other in a small area. The density of elephants in our study area was low (<0.4/ km2) compared to that of other areas (1-4/km2) where detailed elephant studies have been carried out. I could not carry out this analysis because there were groups that did not have radio-collared individuals overlapping with our study animals. However, I noticed that even though three radiocollared female groups were in the general vicinity during the dry season, I located them together only once in two years of tracking. There seems to be very little temporal overlap between the female groups within the study area. Summer ranges were smaller than other seasons due to the limited availability of water in the study area in that season (Tables 3 & 4). The temperatures in the study area rose as high as 42C during summer. Elephants showed a greater fidelity in the dry season than in the other seasons, except for Female K who showed a high degree of fidelity across all seasons. Females remained near permanent water sources during summer, as it would probably be detrimental to the survival of calves to move widely in search of food during such temperatures. Also the females with young calves (D, M and K) used permanent water sources in areas with fewer disturbances. This is consistent with other studies on African elephants where water was a limiting factor (Leuthold 1977; Viljoen 1989a; Thouless 1995). Elephants in this area also showed a high degree of fidelity across dry and wet seasons, which was in contrast to the elephants of Tsavo (Leuthold 1977). Another point to note in the present study was that both Females D and M changed their ranging pattern from previous years immediately following the birth of a newborn calf. Thus this study also proves that elephants show considerable flexibility in ranging behavior to improve their chances of survival. Very few studies (Joshua & Johnsingh 1995) have reported increases in seasonal ranges due
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to adult males coming into musth. While Males T and A came into musth in winter, male S came into musth in summer. I found that all three adult males that I followed were given to wandering widely in search of females during musth and consequently had large ranges (Table 3) during musth when compared to other seasons. In the rainy season of 1997-98, Male T shifted between two areas and hence a large home range was recorded. Similarly, Joshua and Johnsingh (1995) reported that a male, which was radio-tracked for over two years, increased its seasonal range from 22 km2 in the monsoon to over 200 km2 in winter (its musth season). Elephants in the population seemed to use Shorea-mixed vegetation type much more than the other vegetation types (Williams unpublished data). This seems to be consistent even with selection at an individual level, where Shorea-mixed vegetation was used in proportion to availability. This is the vegetation type with the highest diversity of elephant food plants. Shorea vegetation had the lowest dung densities indicating minimal elephant use (Williams unpublished data). However, individual elephants with young calves, that were radio tracked for over two years, showed strong selection for the Shorea vegetation. This is mainly due to the fact that very few species appropriate for pruning by humans to use as cattle fodder are found in this vegetation type. They are therefore avoided by the Gujjars to a large extent, and thus less disturbed than the other vegetation types (Williams, Johnsingh & Krausman 2002). During the monsoon season, females and males used the miscellaneous vegetation in proportion to availability or selected it in a few cases. I believe this is due to the abundance of green grasses like Dolichostachya and the presence of the bamboo Dendrocalamus strictus, important food sources for elephants during the monsoon. Elephants in the study area eat a large amount of grass in the wet season, even if they appear to like browse at other times; this seems to be consistent with studies in Africa (Buss 1961; Field 1971; Laws, Parker & Johnstone 1975; Viljoen 1989b). Seasonal changes in habitat selection and diet have been observed in different elephant populations across Africa and Asia (Buss 1961; Field 1971; Mckay 1973; Laws et al. 1975; Leuthold 1977; Olivier 1978; Barnes 1982; Sukumar 1991; Sivaganesan & Satyanaranyana 1995), indicating the relative opportunistic nature of the diet of elephants. They are able to utilize a wide selection of foods available from the ground up to four to five meters and thus are able to survive even harsh environmental conditions. The distribution and availability of water governs the distribution of elephants (Laws 1970; Kerr & Fraser 1975). Outside of the monsoon season, water availability in the study area is restricted to a narrow belt along the slopes of the hills. In summer, water availability becomes truly restricted to small pools. Yet I failed to detect any differences in distance to water between the winter and summer seasons for the study animals, suggesting that elephants used areas nearer to water at all times. This study has demonstrated clearly that a major influence on ranging and habitat use in the study population is food plant diversity and density for the general population, while it is disturbance for females with calves at heel. Musth behavior was the primary driving factor for large home ranges of fully grown adult males. Female elephants with calves do not tolerate disturbance at all and females respond to disturbance by moving into areas with less disturbance. Implications for Asian elephants in captivity Captive facilities should make arrangements for a large, screened-off area for pregnant females and females with calves, thus reducing the disturbance factor from visitors and other noise. Young adult females learn about calving by helping older females during and after birth and thus opportunities should be given to younger females to be around a calving female in order to exploit those
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opportunities to learn. Elephants also like a wide variety of food and range widely in search of food. Thus, allowing elephants to range in large sanctuary-like areas would allow them to explore and exhibit the natural foraging and social behaviors that are seen in their wild relatives, but are suppressed while in small captive enclosures. Males, on the other hand, roam widely when in musth in search of females. Tragic consequences result when this behavior is disrupted, through barriers, enclosures or human disturbance, and has resulted in the killing of mahouts and handlers. However, I have never felt threatened when approaching a musth bull in the wild who has free access to female elephants. A musth elephant guarding a female will only charge someone who gets too close for a short distance before going back to guard the female. Therefore, the community holding captive male elephants needs to apply the bold idea of keeping adult elephant bulls free from chains and restraints, and having access to females in a larger, secure area. This would allow adult bulls to exhibit normal ranging behavior and not become dangerous because of sexual frustration at being tied down when their testosterone levels are so high. Acknowledgments I thank the Officers of the Uttaranchal Forest Department, the Additional Inspector General of Forests (Wildlife), Ministry of Environment and Forests, Government of India and Director, Project Elephant, Government of India who granted the permissions for this study. I also wish to thank the faculty and staff at the Wildlife Institute of India and the University of Arizona who helped me during analysis and write up of my Ph.D., which led to this manuscript. The U.S. Fish and Wildlife Service funded this project and I particularly thank Dave Ferguson and Fred Bagley for all the encouragement and support rendered to carry out this research. References
Barnes RFW. 1982. Elephant feeding behavior in Ruaha National Park, Tanzania. Afr J Ecol 20:123-136. Baskaran N, Balasubramanian M, Swaminathan S, Desai AD. 1995. Home range of elephants in the Nilgiri Biosphere Reserve, South India. In: Daniel JC, Datye HS, eds. A week with elephants. Bombay, India: Bombay Natural History Society, Oxford University Press. p. 350-367. Buss IO. 1961. Some observations on food habits and behavior of African elephants. J Wildl Manage 25:131-148. Byers CR, Steinhorst RK, Krausman PR. 1984. Clarification of a technique for analysis of utilizationavailability data. J Wildl Manage 48:1050-1053. De Villiers PA, Kok OB. 1997. Home range, association and related aspects of elephants in the eastern Transvaal Lowveld. Afr J Ecol 35:224-236. Douglas-Hamilton I. 1972. On the ecology and behavior of the African elephant. Ph.D. Thesis. University of Oxford, Oxford, UK. Field CR. 1971. Elephant ecology in the Queen Elizabeth National Park, Uganda. E Afr Wildl J 9:99-123. Hooge PN, Eichenlaub B. 1997. Animal movement extension to arcview. ver. 1.1. Alaska Biological Science Center, U.S. Geological Survey, Anchorage, AK, USA. Jachmann H. 1992. Movements of elephants in and around the Nazinga Game ranch, Burkino Faso. J Afr Zool 106:27-37. Johnsingh AJT, Prasad SN, Goyal SP. 1990. Conservation status of the Chilla-Motichur corridor for elephant movement in Rajaji-Corbett National Park area, India. Biol Cons 52:125-38. Joshua J, Johnsingh AJT. 1995. Ranging patterns of elephants in Rajaji National Park: implications for reserve design. In: Daniel JC, Datye HS, eds. A week with elephants. Bombay, India: Bombay Natural History Society, Oxford University Press. p. 256-260.

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Kemf E, Santiapillai C. 2000. Wanted alive! Asian elephants in the wild. 2000 WWF Species Status Report. Gland, Switzerland: WWF-International. Kerr MA, Fraser JA. 1975. Distribution of elephants in a part of the Zambezi Valley, Rhodesia. Arnoldia Rhodesia 7:1-14. Laws RM. 1970. Elephants as agents of habitat and landscape change in East Africa. Oikos 21:1-15. Laws RM, Parker ISC, Johnstone RCB. 1975. Elephants and their habitats: the ecology of elephants in north Bunyoro, Uganda. London, UK: Oxford University Press. Leuthold W. 1977. Spatial organisation and strategy of habitat utilization of elephants in Tsavo National Park. Z Saugetierkunde 42:358-379. Mares MA, Willig MR, Bitar NA. 1980. Home range size in eastern chipmunks, Tamias striatus, as a function of number of captures: statistical biases of inadequate sampling. J Mamm 61:661-669. Matthiessen P. 1992. African silences. New York, NY: Random House. McKay GM. 1973. Behavior and ecology of the Asiatic elephant in southeastern Ceylon. Smithsonian Contributions to Zoology. Vol. 125. Washington DC: Smithsonian Institution. Mohr CO. 1947. Table of equivalent populations of North American mammals. Am Midland Natur 37:223249. Olivier RCD. 1978. On the ecology of the Asian elephant with particular reference to Malaya and Sri Lanka. Ph.D. Thesis. University of Cambridge, Cambridge, UK. Santiapillai C, Jackson P. 1990. The Asian elephantan action plan for its conservation. IUCN/SSC Asian Elephant Specialist Group. Gland, Switzerland. Singh KN. 1995. Asiatic elephants in Uttar Pradesh (India): status and strategy for conservation. In: Daniel JC, Datye HS, eds. A week with elephants. Bombay, India: Bombay Natural History Society, Oxford University Press. p. 32-48. Sivaganesan N, Sathyanarayana P. 1995. Mortality of trees caused by elephants in Mudumalai Wildlife Sanctuary, South India. In: Daniel JC, Datye HS, eds. A week with elephants. Bombay, India: Bombay Natural History Society, Oxford University Press. p. 132-148. Sukumar R. 1991. The Asian elephant: ecology and management. Cambridge, UK: Cambridge University Press. Tchamba MN, Bauer H, De Jongh HH. 1995. Application of VHF-radio and satellite telemetry techniques on elephants in northern Cameroon. Afr J Ecol 33:335-346. Thouless CR. 1995. Long distance movements of elephants in northern Kenya. Afr J Ecol 33:321-334. Thouless CR. 1996. Home ranges and social organisation of female elephants in northern Kenya. Afr J Ecol 34:284-297. Viljoen PJ. 1989a. Spatial distribution and movements of elephants (Loxodonta africana) in the northern Namib Desert of the Kaokoveld, South West Africa/Namibia. J Zool Lond 219:1-19. Viljoen PJ. 1989b. Habitat selection and preferred food plants of a desert-dwelling elephant population in northern Namib Desert, South West Africa/Namibia. Afr J Ecol 27:227-240. Whyte I. 1996. Studying elephant movements. In: Kangwana K, ed. Studying elephants. African Wildlife Foundation, technical handbook series 7. Nairobi, Kenya: African Wildlife Foundation. p. 75-89. Williams AC, Johnsingh AJT, Krausman PR. 2002. Elephant-human conflict in Rajaji National Park. Wildl Soc Bull 29(4):1097-1104. Williams AC, Johnsingh AJT, Krausman PR. In press. Population estimation and demography of the Rajaji National Park elephants, northwest India. J BNHS. Worton BJ. 1989. Kernel methods for estimating the utilization distribution in home-range studies. Ecol 70:164-168.

51

A. Christy Williams is a large-mammal biologist who conducted his Ph.D. from the Wildlife Institute of India on Elephants and their habitats in Rajaji National Park. He has continued to study the population parameters of this elephant population since he began the study in 1996. Currently he coordinates the WWF Asian Elephant and Rhino Conservation program that is being implemented in eight Asian countries. He is also involved in active research in Borneo, Malaysia and Sumatra, Indonesia, where he is helping range-country biologists study elephants using GPS-equipped satellite collars. He may be contacted at: c/o WWF Nepal Program, P.O. Box 7660, Baluwatar, Kathmandu, Nepal or at the Wildlife Institute of India, P.O. Box 18, Dehra Dun 248001, India. Email: acwill69@yahoo.com.

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Introduction
Robert P. D. Atkinson Head of Wildlife Department The Royal Society for the Prevention of Cruelty to Animals Health and welfare differ from each other. A person or animal may be in good physical health, yet suffer from poor welfare if they are psychologically unwell. The measurement and restoration of physical health has traditionally been the province of veterinarians, such as three of the authors in this section, Gretchen Kaufman, Janet Martin and Susan Mikota, whereas behaviorists and psychologists like Gay Bradshaw concentrate on psychological illness and treatment. Yet increasingly the two areas are beginning to overlap, yielding an exciting area of study that embraces a holistic approach to well-being and illness. The authors in this section all recognize elephants as a model species to which this approach can be applied. First, there is a view commonly held among those who study them that elephants well-being may be deeply affected by key events in their lives, particularly those that concern their social and physical environments. Bradshaw develops this view into a disturbing hypothesis, that the trauma of elephants capture, separation from family and subsequent confinement predisposes them to a wide variety of physical, psychological and behavioral problems. Kaufman and Martin urge that the assessment of health begin with a comprehensive audit of all aspects of welfare, from failure to reproduce through to oral health problems, and then proceed to the identification and, ultimately, treatment of the underlying factors. Finally, Mikota sends out a clear caution on the dangers of tuberculosis to captive and wild elephants, as well as to humans. She makes a compelling case that the stresses captivity can place on elephants may heighten their susceptibility to the disease, a caution caretakers would do well to heed given the high percentage of their elephants that test positive to TB. Whatever the cause, it is clear that something is wrong with the health of many captive elephants. The problems captive elephants caregivers have to deal with such as stereotypy, chronic weight and foot problems, infertility and infanticide, are hardly known in wild elephants where human interference is minimal or absent. The issues covered in this section serve as a sharp reminder to us all that the welfare of the animals our societies keep captive is the concern of us all. As Kaufman and Martin so clearly state, the health of elephants in zoos is not only the business of their caretakersit is the responsibility of the society that demands that zoos keep elephants.

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Chapter 4 Inside Looking Out: Neuroethological Compromise Effects in Elephants in Captivity


G. A. Bradshaw

The Kerulos Center Pacifica Graduate Institute Oregon State University The Brain is wider than the Sky Forput them side by side The one the other will contain With easeand youbeside. Emily Dickinson Animal rights supporters are careful to employ the phrase animal in captivity in lieu of the more compact captive animal. This may seem like a circuitous way to make an obvious point: captivity does not a captive animal make. But, obvious or not, the distinction is neither prevalent in practice nor concept: captivity has not been understood as a condition that seriously changes a wild animal. What we understand today says otherwise. Biomedical research has demonstrated that the effects of psychological distress are equal to the costs of physical pain and damage, and, in many cases, much more enduring and difficult to heal (van der Kolk, McFarlane & Weisaeth 1996). What we experience psychologically penetrates deep within (Sapolsky 2004). Further, such vulnerability to stress and trauma is shared by all vertebrates (Panksepp 1998; Berridge 2003; Bradshaw & Schore 2007). Today, with this knowledge, investigators work increasingly from the assumption of a common model of mind and body for both humans and animals (see Panksepp 1998; Berridge 2003; Bradshaw & Finlay 2005; Daston & Mitman 2005; Bradshaw & Sapolsky 2006; Wrangham, Wilson & Muller 2006). This represents a significant advance in our ability to assess elephant well-being. While considerable attention has been given in recent years to the physical and social hardships elephants endure in captivity (e.g., Clubb & Mason 2002; Brown, Wielebnowski & Cheeran 2005), little to no attention has been given to their function as psychologically-mediated stressors. Any venture into the realm of subjective (psychological) animal experience was considered to lack an accepted theoretical framework, and was usually met with dismissive criticisms of anthropomorphism. Now, a new trans-species science has emerged (Bradshaw & Sapolsky 2006). Psychology, ethology and neurobiology have come together into a coherent, cross-species model of brain and behavior: trans-species psychology (Bradshaw & Watkins 2006; Bradshaw & Schore 2007). This means it is possible to take what is known about humans into investigations of other species (see
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Brne, Brne-Cohrs & McGrew 2004; Brne, Brne-Cohrs & McGrew 2005; McMillan 2005; Brne, Brne-Cohrs, McGrew & Preuschoft 2006; Fabrega 2006; Bradshaw, Capaldo, Lindner & Grow 2007). In the case of assessing elephants in captivity, a wealth of studies documenting psychobiological stress effects on health and well-being now has been made available along with detailed studies that underscore parallels between human and elephant neuroethology (Hakeem, Hof, Sherwood, Switzer et al. 2005; Hart, Hart, & Pinter-Wollman in press). Relationships between trauma, stress and underlying neural substrates are considered relatively well understood not only because of the amount of data amassed but also because subjective/psychological and objective/neurophysiological processes are linked in mechanistic models (van der Kolk et al. 1996; Yehuda, Engel, Brand, Seckl et al. 2005). Cross-species models of the mind achieve greater scientific coherence and simultaneously compel a concomitant ethical shift in scientific practice (Bradshaw, Capaldo, Lindner & Grow 2007). The latter distinguishes trans-species psychology from the traditional field of comparative psychology. Trans-species psychology and comparative psychology both involve the study of the mind and behavior across species. However, trans-species psychology understands the study of animal psyche as a goal unto itself and not as a tool or model primarily directed toward elucidating the human mind. Further, trans-species psychology is a psychology of all vertebrates rooted in a single psychobiological model, not the concatenation of a core animal mind covered with a human veneer (Bradshaw & Finlay 2005). Similar to psychology in general, trans-species psychology is committed to the health and well-being of its subjects, who, by definition, include all species. Tran-species psychology is therefore rooted in methods and enquiry that eschew causing distress or damage in the process of knowledge-making. In so doing, a clinical assessment of the well-being of elephants in captivity simultaneously engages an evaluation of the institutions involved that affect elephant health. By expanding definitions of health to include the psychological, we bring attention to the striking parallels exhibited between humans and elephants experiencing captivity. Here, elephant experience in captivity is examined through this lens with specific attention to the etiology, mechanisms and symptoms of Complex Post-Traumatic Stress Disorder (Complex PTSD) that are defined by and associated with conditions of forced confinement (Herman 1997, 2004). Mammalian neuroethological development Like other obligate social vertebrates, elephant1 young are immersed in a relational environment. Elephant life is best imagined as a field or web of relationships and interactions in which individuals are embedded and connected to each other. Attachment (i.e. caregiver-infant bonding: Stamps 2003) is the first stage in a series of socialization processes. As the central feature of the natal herd it represents a formative process of elephant society. Multiple studies on diverse species have
1. Certain terminological conventions will be observed. The term captivity is used to refer to close confinement captivity in contrast with free agency captivity. The latter refers to captive conditions practiced and structured at two North American elephant sanctuaries, The Elephant Sanctuary in Tennessee (TES; http://www.elephants.com and the Performing Animal Welfare Society (PAWS; http://www.paws.org) that provide expansive natural environmental settings for elephants, and refrain from employing domination or control either through manipulation (e.g., enforcing a certain living regimen, free contact) or force (e.g., use of ankus, prods, chains). The terms free-ranging and wild are used interchangeably here to denote conditions and behaviors considered sufficiently normative and consistent with conditions and behaviors that existed prior to colonial settlement of elephant lands. Further, elephant refers to Asian (Elephas maximus) and African savanna (Loxodonta africana) species because the level of analysis here is considered to hold equitably for both. 56

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shown the importance of extended maternal care (Rheinhold 2002; Sullivan 2003). Parents or alloparents (i.e. a set of affiliated sibling and adult caretakers: Lee 1987) provide the primary external source of sensory input and regulation of all essential developmental processes that interact with genetics and greater environmental conditions (West & King 1987; West, King & White 2003). Relational qualityhow and with whom an infant experiences interactions sociallydeeply affects individual viability and adaptation success over the rest of the life span (Schore 1994). Early social contexts are comprised of multiple dynamic processes having the potential for positive or negative values in terms of ecological and evolutionary significance (Stamps 2003). Socialization quality influences fitness by affecting infant protection, stress levels, resource mobilization and socio-ecological knowledge (Mesnick 1997). For example, elephant matriarch age is a significant predictor of the number of calves produced by the family (McComb, Moss, Durant, Sayialel et al. 2001). Levels and quality of sociality among adult females have been positively correlated with infant survival in primates and other species (e.g., elephants: Lee 1987; baboons: Silk, Alberts & Altmann 2003). Patterns of socialization are mirrored in the process of brain development. By definition, brain development is relational (Siegel 1999). Social context parameters directly influence one of the most fundamental structures in behavior regulationthe hypothalamic-pituitary-adrenal (HPA) axis. Social behavior associated with the HPA axis acts to increase right hemisphere dominance, the role of which has become increasingly appreciated in the study of mammalian behavior (Tang, Reeb, Romeo & McEwen 2003). Preferential hemispheric development is significant because, post-natally, maturing orbital prefrontal areas in the early developing right brain are centrally involved in attachment, emotion, stress regulation and the control of social behavior (Schore 2005). Highly complex behaviors such as self-awareness and grieving (e.g., Douglas-Hamilton, Bhalla, Wittemyer & Vollrath 2006; Plotnik, deWaal & Riess 2006) are related to attachment quality and right brain development (Cutting 1992; Schore 2002, 2003a). Consequently, when we see interactions between an infant and his/her mother, allomothers and other offspring, we are witnessing the dialogical process between sociality and neurobiology. The social context of the elephants natal herd, and the infants own autonomic nervous system (ANS), function as the basic regulatory mechanisms that shape neural substrates and associated behavior. Essentially, the social context tunes the infants stress responses through neuroethological patterning and even through tissue-specific effects on gene expression (Meaney & Szyf 2005). The infants sense of self, emplacement and function are calibrated to the socio-ecological surround in which s/he is raised. Stress effects on brain-behavior development The sensitivity of the mammalian brain to socio-ecological context cannot be minimized. Transactions can be either positive to the organism (i.e. growth-promoting) or negative (i.e. growthinhibiting) depending on the quality of the experience or stressor (Schore 1994). In its most general definition, stress is experienced through a differential between an individual and the environment. Stress is defined as the non-specific response of the body to any demand (Selye 1984) and is not considered detrimental until the psychobiological envelope to which every species, and individual, is evolutionarily and ecologically adapted, is exceeded. When this adaptive threshold is breached, there is the potential for traumatic psychological and physiological damage. Traumatic stress is distinguished from other stress in that it is defined as physically or emotionally inflicted injury that is perceived by an individual or a group to threaten their existence (van der Kolk et al. 1996). Trauma differs from other diagnoses in that it includes not only the
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symptoms but also the precipitating source. Post-Traumatic Stress Disorder (PTSD) is unique in the DSM-IV2 in that it is one of the only two disorders (the other being Reactive Attachment Disorder) that includes as part of its definition the cause of presenting symptoms (American Psychological Association 2002). Accordingly, the diagnosis of PTSD in elephants in captivity is firmly rooted in definition, causation and observation. Traumatic disruption of normative social bonding patterns from a single threatening event can create lifelong changes in social learning abilities and neural organization (Wiedenmayer 2004). Direct (e.g., death of mother) or indirect (e.g., transmitted maternal stress: Francis, Diorio, Liu & Meaney 1999) compromise can induce sustained effects on brain plasticity, thereby creating a structural vulnerability for psychopathogenesis and early death (Cirulli, Berry & Alleva 2003). Early attachment trauma is thereby affectively burnt in the limbic system and the HPA axis (Stuss & Alexander 1999). Altered sociality translates to altered patterns in core survival functions that govern basic coping behavior and stress regulation abilities (Perry & Azad 1999). These include knowing how to behave appropriately in intra- and inter-specific encounters. Further, by such mechanisms, trauma or stress that occurs during gestational and postnatal periods can transmit to and influence functioning of the offspring (Dettling, Feldon & Pryce 2002). Negative or excessive stress effects manifest both intra-organismically (e.g., increased vulnerability to disease, immunological compromise: Sapolsky 2004) and inter-organismically (e.g., asocial and atypical affiliative behaviors: Schore 2003a) by triggering hyperarousal in the limbic and autonomic nervous systems that support emotional behavior. Resulting impairment of socioaffective circuits, especially in higher cortical regions, underlies many abnormal and inappropriate emotional responses that express at later stages of life (Poeggel, Nowicki & Braun 2005). This is biochemically expressed in elevated levels of arousal-regulating catecholamines, corticotropinreleasing factor and corticosteroids, and behaviorally in one or more ways: a persistent fearful temperament (Adolphs, Gosselin, Buchanan, Tranel et al. 2004); diminished capacity to modulate memory, fear and social judgment; a predisposition to aggression dysregulation and violence; and PTSD (Raine, Park, Lencz, Bihrle et al. 2001; Schore 2003a, b; Morris & Dolan 2004). Complex PTSD and the psychology of captivity While common processes and mechanisms underlie the trauma response, comparative research indicates that PTSD as defined in the DSM-IV captures only certain symptoms and etiologies of trauma. Studies on a diversity of individuals (e.g., concentration camp survivors: Krystal
2. The diagnosis of post-traumatic stress disorder (PTSD) is defined by the Diagnostic and Statistical Manual of Mental Disorders - Text Revision (American Psychiatric Association [APA], 2002, p.332): The essential featureis the development of characteristic symptoms following exposure to an extreme traumatic stressor involving direct personal experience of an event that involves actual or threatened death or serious injury, or other threat to ones physical integrity; or witnessing an event that involves death, injury, or a threat to the physical integrity of another person; or learning about unexpected or violent death, serious harm, or threat of death or injury experienced by a family member or other close associate (Criterion A1). The persons response to the event must involve intense fear, helplessness or horror (or in children, the response must involve disorganized or agitated behavior) (Criterion A2).The characteristic symptoms resulting from the exposure to the extreme trauma include persistent re-experiencing of the traumatic event (Criterion B), persistent avoidance of stimuli associated with the trauma and numbing of general responsiveness (Criterion C), and persistent symptoms of increased arousal (Criterion D).The full symptom picture must be present for more than one month (Criterion E), and the disturbance must cause clinically significant distress or impairment in social, occupational or other important areas of functioning (Criterion F). 58

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1978; veterans and prisoners of war: Bremner, Southwick, Brett, Fontana et al. 1992; and victims of domestic violence: Burgess & Holstrom 1974; Rollstin & Kern 1998; van der Kolk 2004) have suggested a more comprehensive system for classifying profound psychological disturbances where events and their responses span a range of forms along a continuum (Briere & Spinazolla 2005). At one end of the complexity continuum are individuals who have experienced healthy, loving rearing and childhoods, and exhibit what are considered normal stress and affect regulation capacities, but are suddenly confronted with a single terrifying incident (e.g., adult-onset, singleincident experiences such as a car accident). At the other end of the spectrum are individuals who have sustained early onset, prolonged or multiple, highly invasive and repeated traumatic events and who, for a variety of reasons, may be more vulnerable to stress effects (Briere & Spinazzolla 2005). The latter includes children, prisoners and others who are unable to escape their circumstances emotionally and physically or both and who typically develop more complicated and enduring presentations (Herman 2004). In recognition of the extraordinary and complicated psychological conditions that captivity entails, trauma researchers have defined a specific diagnostic category: Complex PTSD (Herman 1997, 2004). Explicit acknowledgment of the difference between prolonged, repeated psychophysical assaults and a single traumatic event has brought deeper insights into the nature and mechanisms of psychological disturbances. The effects of forced confinement have not always been appreciated even in the case of humans. There has been a propensity to fault the character of the victim even in the case of politically organized mass murder[as in] the aftermath of the Holocaust that witnessed a protracted debate regarding the passivity of the Jews and their complicity in their fate (Herman 1997, p. 115). But, as Herman points out, these are concepts that hold only to the situation of free will. By definition, forcible confinement relocates an individual into a completely different environment and in so doing creates a second reality for the prisoner. Day-to-day survival, and even meaning-making (sensu Frankl 1946), become referenced to the coordinates of the captive world. We encounter two key themes in studying the effects of captivity: the experience of forced physical confinement and the distortion of core relational processes and structures to which the prisoner is subjected. First, let us examine what physical confinement means. Each one of us is limited in some way in our ability to move about freely in space. For instance, there are places, such as the Pentagon or restrooms of the opposite gender, from which we are excluded. And even though the actual dimensions of everyday life stay within a predictable spatial routine, and we may rebel against the tethers that postmodern life imposes, such delineations do not usually constitute true confinement. In most captive situations, prisoners live in highly depauperate and restricted environments where they are denied even the possibility of exercising free will. Captivity is a psychologically mediated physical condition that disbars agencythe sense of self as an instrument of ones own destiny (Herman 1992, 2004). Further, because it generally involves more than physical structures (i.e. there is a living presence maintaining confinement) captivity entails not only the denial of agency but its forced transfer to the captors authority. Physical violence is typically employed to render initial confinement. As time progresses, confinement, aided by memory and reminders of physical harm, evolves into a tool specifically intended to increase psychological control (Herman 2004). It is the victims total dependence on the person in power that corrodes their sense of self-efficacy, and their ability to survive, let alone resist (Krystal 2004). Thus, through captivitys reduced physical environment and the secured, complete dependence on the captor, the prisoner loses relational connection with the essential fabric of psychological living.
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Social isolation and ecological stripping through institutional living translate to feelings of psychological powerlessness. Human trauma survivors, such as Jacobo Timerman (2002), underscore how captive life erases a connection with the future and the past and instills a sense of helplessness and hopelessness (Herman 2004; Krystal 2004). Whether enforced physically or psychologically, confinement forces the captive to maintain focus on the present moment and disallows core functions that maintain a healthy sense of self and an ability to relate to others. Studies show that when human prisoners are group-housed, there is an opportunity to have what traumatologists refer to as the basic unit of survivala companion (Luchterhand 1980; Herman 1992). However, the highly unpredictable, threatening atmosphere and omnipresence of potential annihilation that is conveyed through the dissolution of identity and community, can even extinguish interpersonal relationships and produce violence or indifference, even towards family members (Weisel 1958). When inner autonomy, world view, moral principles, or connection with others for the sake of survival are relinquished (Herman 2004) there is a shutting down of feelings, judgment, and initiative leading to robotization (Krystal 1978). Taken more broadly, where normative well-being is envisioned as a function of a thriving set of nested social and ecological relationships, captivity translates to a process where critical functions of psychobiological attachment and meaning are ruptured and damaged. Captivity as an institution of relational trauma We now examine elephant captivity through the lens of traumatology. In beginning to assess another species, particularly in a comparative context, it is helpful to define a baseline outside captivity. Captive life is therefore framed in consideration of what we understand to be normative socio-ecological conditions for elephants. Levels and quality of stress which elephants sustain in confinement may be estimated by assessing the difference between wild and captive conditions. Many authors have written extensively on wild/captive contrasts in such variables as attachment and social processes, food type, variety, and availability and habitat and how they significantly exceed the evolutionary and ecological envelope of conditions to which elephants have adapted (see Bradshaw & Lindner 2006; Bradshaw 2007; Kane, Forthman & Hancocks, Appendix I; Kinzley, Chapter 12; Lee & Moss, Chapter 2; Poole & Granli, Chapter 1). From the perspective of developmental neuroethology, capture, captive breeding and a life of close confinement severely challenge elephant psychobiology. Wild-caught elephants sustain a series of traumas: shock trauma from the cull/capture experience, relational trauma from premature weaning and compromised rearing, loss of primary attachment structures and processes with separation from his/her mother and natal herd, stress from transport and translocation, and hardship from environmental deprivation in confinement (Bradshaw, Schore, Poole, Moss et al. 2005; Bradshaw & Schore 2007). Individuals born in captivity are born to mothers who are living under highly stressful conditions and they are therefore susceptible to stress-transmission during gestation. After birth, young captive-born elephants typically lack the traditional allomother-rearing context, are often separated from mother and live alone or in highly altered social structuressimilar to traumatic stress conditions that have been linked with serious and functional compromise elsewhere and significantly affect elephant well-being and behavior (see Poole 1989; Gara 1997; Nyakaana, Abe, Arctander & Siegismund 2001; Gara, Slotow, Carr & Reilly 2004; Bradshaw et al. 2005; Bradshaw & Schore 2007; Kurt & Gara 2007). Given that formative physiological and psychobiological maturation occurs within the first decade or more of life and through a complex
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of relationships (e.g., allomothers: Lee 1987; see Fleming, ODay & Kraemer 1999), disruptive experiences defining captivity both constitute a major departure from historically free-ranging elephant society and from normal brain-behavior development (Bradshaw & Schore 2007). Capture and captive birth closely conform to specific criteria that are identified as precursors to reactive attachment disorders or PTSD (APA 2002). For example, wild-caught elephants forcibly removed from their families are exposed to an extreme traumatic stressor involving direct personal experience of an event that involves actual or threatened death or serious injury (Criterion A1). Asian and African elephants who are brought into captivity have witnessed an event that involves death, injury, or a threat to the physical integrity of anotherunexpected or violent death, serious harm, or threat of death or injury experienced by a family member or other close associate and respond to the event with intense fear, helplessness, or horror (Criterion A2; APA 2002). Brain imaging research shows that major neuroethological compromise can extend well beyond infancy. In the case of bull elephants, this may have particular significance. Given social and neurobiological parallels among the mammalian species, and the specifics of male brain development (Taylor 1969), elephants likely undergo a second phase of brain development through their teen years. However, because of fear of injurious aggression, bulls in captivity are separated at an early age from their mothers and most often are kept isolated or significantly distanced from other elephants, thereby missing the second phase of socialization of an all-male herd or area and adding to dysfunctions introduced early on. Similarly, females in captivity are almost always separated from family members and are often removed from conspecifics for years (e.g., Maggie, Anchorage, Alaska Zoo), or housed with non-family members and sometimes with another species. Increasingly, detailed analyses of wild elephants indicate that core elephant social dynamicsand hence fitness and viabilityare strongly influenced by genetic relatedness (Archie, Moss & Alberts 2006). Elephants are often transferred between zoos or from circuses to zoos, thereby disrupting any stabilizing, intra- or inter-specific social bonding that may have developed. Many zoos make efforts to increase biophysical and social diversity, but given physical and logistical limitations of structures and practices of close confinement, elephant life remains completely or largely determined by the agendas of zoo personnel. There is little opportunity for revitalizing agency that is, by definition, seriously undermined in captivity. Personal exercise of free will is highly circumscribed within a narrow set of parameters (e.g., availability of enrichment toys and activities), time, and space. Quotidian routines with little variety relative to wild conditions and continued atrophy of agency leads elephants, as Timerman (2002) describes, to robot-like behavior and numbing which may appear as loss of appetite, depression, stereotypy and apathy (e.g., see Forthman 1998; Clubb & Mason 2002; Schmidt 2002; Brown et al. 2005; Kane et al., Appendix I). The combination of stressorsphysical hardship, social isolation or limited and irregular interactions, total dependence on the caretaking personnel and (often) punishment or negative reinforcementcreates chronic stress and trauma consistent with what are considered to be precipitants of Complex PTSD (Herman 1997; van der Kolk, Roth, Pelcovitz, Sunday et al. 2005). Again consistent with cross-species studies on trauma, many elephants in captivity show a constellation of trauma-induced physical, psychological and behavioral symptoms. The demands of captivity also result in symptoms that are complex, diffuse and tenacious (Herman 1997, 2004), where specific presentations manifest relative to the age at which the trauma (first) occurred and the number of traumatic experiences suffered subsequently (van der Kolk et al. 2005). Thus, while broad patterns of symptoms are statistically evident, differences in gender, age, details of capture and captive conditions and personality account for specific presentations in an individual. For
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example, some affective disorders in female elephants may appear less obvious compared with males (i.e. female-internalizing (depression) versus male-externalizing (hyper-aggression): Bradshaw & Schore 2007). The consequences of an elephants inability to adapt successfully to such conditions attest to the costs of captivity. While commonly observed in elephants in captivity, stereotypic behavior has never been reported in over 34,000 sightings of wild elephant groups containing 1 to 550 individuals. Further, there are no observations of chronic foot or weight problems in the Amboseli elephant population, consisting of over 2,200 individuals. Out of 1,500 births observed in the wild, there were no cases of infanticide or calf rejection. Similarly, there have only been two cases of infertility out of 558 females over 10 years of age (C. Moss, AERP long-term records; Lee & Moss in press; Moss & Lee in press). In contrast, a survey by In Defense of Animals of 35 zoos involving 135 elephants showed that 62 percent and 42 percent of the elephants have severe foot disease and joint disorders, respectively. There were 60 stillbirths and out of 15 live births, 73 percent experienced complications during birth and 25 percent of the individuals had reproductive disorders. Other symptoms include decreased longevity, auto-immune disease, unanticipated aggression, depression, intra-specific aggression, stereotypy and infanticide, all of which are observed commonly in elephants kept in close confinement (see Kane et al., Appendix I). Behavioral symptoms include personality disorders, poor social skills or asociality, loss of impulse control, hyperarousal and unpredictable outbursts, and a high vulnerability to self-injury. Dissociative or dissociative-like behaviors are commonly observed in elephants who are confined (e.g., somatization, swaying and other stereotypies). It is not surprising that elephants in captivity exhibit behavioral sequelae (e.g., intra- and inter-specific hyper-aggression, self-injury3, anhedonia, infant rejection and injury) similar to other species, humans included, under parallel conditions (Bradshaw & Schore 2007). Intra-specific violence, such as the extraordinary event at the Tel Aviv, Israel Zoo in 2007, in which a 36-year-old bull killed a 46-year-old cow elephant, is consistent with symptoms of hyper-arousal, neuroendocrine compromise and stress dysregulation associated with Complex PTSD (Herman 2004; Panksepp & Zellner 2004; Schore 2005). Such behavior, so radically unprecedented in the historic wild, is reminiscent of the violence a severely traumatized individual may show toward family members whom they have cherished and loved prior to their incarceration and torture (Weisel 1958). Much is made of the elephant-human relationship in captivityindeed, cultivation of this bond is considered key to successful management of elephants in captivity. But as traumatologists are quick to point out, these relationships are psychologically corrosive and volatile because of the imposed power differential: the human plays the dual role of agent of captivity or abuse or both, as well as attachment and survival. Elephant management is by definition physical (e.g., ankus, chutes) and emotional (e.g., trainer-elephant relationship) coercion (Kane et al., Appendices I & II). The elephant-human relationship in closed confinement captivity therefore embodies perennial potential for re-traumatization that can lead to symptoms such as sudden outbursts and flashbacks or precipitous declines in physical and mental health (Herman 2004; Bradshaw & Lindner 2006).
3. Sadly, many conditions in the wild have become extremely stressful and fearful for many elephants (see Bradshaw et al. 2005; Bradshaw & Schore 2007). However, these locales and situations need to be contrasted with historical conditions when human disturbance was minimal relative to presentthat is, in many places, wild conditions show similar intensity and extensiveness of stress that are observed consistently in captivity. Amboseli, Kenya, is one area that has retained relatively stable conditions but is also extremely precarious and increasingly under human pressures. 62

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Discussion The scientific framework of trans-specific psychology provides a means to clinically assess elephant psychobiological well-being in a manner that is congruent with extant models of elephant behavior and biology. This perspective frames elephant health as a function of social and ecological relational quality; that is, mental and physical health is evaluated relative to the compatibility between present conditions and those to which an elephant is evolutionarily and ecologically adapted. Any sustained or acute departure represents a susceptibility to deleterious stress. A psychobiological perspective reveals that stress and alterations in sociality can have far-reaching consequences that produce maladaptive responses to environmental cues later in life. Further, these effects are not constrained to a single individual but can be transmitted across generations. This analysis has illustrated how trauma-inducing conditions experienced by elephants in close confinement captivity parallel those of cases of human captivity (e.g., political and war prisoners; victims of domestic violence). Certain judgments continue to be the subject of debate (e.g., infanticide as learning impediment, sociobiological advantage or psychopathological behavior). However, there is a growing consensus that an obvious set of symptoms associated with distress deviates statistically from a broad normative standard when compared with wild elephants, and that this set seriously compromises health. Captive conditions are creating a population of psychobiologically impaired elephants, many of whom are likely to be candidates for PTSD and a suite of other tenacious psychological, emotional and physical ailments. Given parallels shared among all vertebrates, and particularly social obligates like humans and elephants, diagnoses of PTSD and Complex PTSD for elephants are as firmly rooted in definition, causation and observation comparable to those of humans. Investigating elephant psychophysiological effects of adverse experiences in captivity is therefore supported by several lines of research. The point concerning parallels between elephants and humans is particularly important in terms of making an accurate diagnosis. In his discussion of the characteristics of a judicious approach to cross-species psychological evaluation, Fabrega (2006) stipulates that symptoms qualify as pathological when: (1) behavior and psychological states are relatively persistent and expressed exclusive of any given specific context; (2) they cause an interruption or significant change in an individuals life arc; (3) they comprise identifiable psychological and somatic distress; and/or (4) they constitute significant behavioral alterations relative to an understood social and cultural space. These criteria are satisfied in most cases of elephants in (close confinement) captivity (see Bradshaw & Lindner 2006). Conclusions Traumatology brings coherence to what has been an uneasy boundary between science and ethics, and human and animal studies. In so doing, it accommodates formal enquiry at the scienceethics boundary by including cultural agents of trauma within its scope of study. It simultaneously engages an evaluation of the institutions involved, but one that can be comfortably grounded in scientific reasoning. From the perspective of neuroethology, captivity itself is the formative source of trauma and threat to ill health. Consistent with human traumatology, trauma prevention is the first step. This entails the cessation of elephant capture and captive breeding, and putting an end to maintaining elephants in close confinement captivity. As much as any other potent ecological stressor, human-caused stress and trauma as exercised through captive conditions operate as agents of
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natural selection. Because captivity effects dramatically decrease overall fitness, the use of captive breeding as a tool for conservation is therefore contraindicated from both a scientific and ethical standpoint. A topic that has not been covered here but is of import, is the question concerning recovery from experiences of severe trauma. Longitudinal studies on human and other species and elephants in sanctuaries (Buckley, Chapter 14; Derby, Chapter 15) show that corrective measures can help arrest or ameliorate many symptoms, but not always and not for every individual (Herman 1992; Sapolsky 2004; Yehuda et al. 2005; Bradshaw & Lindner 2006; Ogden, Minton & Pain 2006). In addition to diverse therapeutic measures that may be applied, there is one key theme essential to recovery. Psychiatrist Henry Krystal, a Holocaust survivor himself, writes: Most of all there is a clear indication that ones resilience is proportional to the capacity to mobilize ones love powers [L]ove represents the survivors self-integrating and self healing powers (Krystal 2004). Elephant society provides testimony to this power and compels that we humans become their adepts. Acknowledgments Special thanks to O. Mein Gans, B. Swart, S. de Rek, D. Bell and D. Forthman for critical comments on an earlier draft and to the editors for support and assistance. References

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Wiedenmayer CP. 2004. Adaptations or pathologies? Long-term changes in brain and behaviour after a single exposure to severe threat. Neurosci & Behav Rev 28:1-12. Wittemyer G, Douglas-Hamilton I, Getz WM. 2005. The socioecology of elephants: analysis of the processes creating multitiered social structures. Anim Behav 69:1357-1371. Wrangham RW, Wilson ML, Muller MN. 2006. Comparative rates of violence in chimpanzees and humans. Primates 47:14-26. Yehuda R, Engel SM, Brand SR, Seckl J, Marcus SM, Berkowitz G. 2005. Transgenerational effects of post-traumatic stress disorder in babies of mothers exposed to the world trade center attacks during pregnancy. J Clin Endocrinol & Metabolism 90(7):4115-4118.

Gay A. Bradshaw is the founder and director of The Kerulos Center (http://www.kerulos.org), co-founder of IAATR (International Association for Animal Trauma and Recovery; http://www.iaatr.org) and author of Elephant Breakdown (Yale University Press: 2008). She holds doctorate degrees in psychology and ecology and is on the faculty at Pacifica Graduate Institute and Oregon State University. Her research and publications, which focus on psychological trauma and recovery in elephants, parrots and chimpanzees, have led to the establishment of the new field of trans-species psychology. She may be contacted at gay.bradshaw@kerulos.org

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Chapter 5 Health as an Indicator of Well-Being in Captive Elephants


Gretchen Kaufman and Janet Martin Cummings School of Veterinary Medicine Tufts University Elephants are wild animals. They have evolved over millennia to survive in the savannas and forests of Africa and Asia. They have developed physiological systems designed to meet conditions defined by these environments. Their evolution has resulted in specific adaptations to local constraints affecting nutrition from available vegetation, distribution and availability of water sources, substrate, climate, predation and presence of disease-causing organisms. In addition, as intelligent animals, they have developed complex and varied social systems that are inextricably linked to their health and success as individuals. In contrast to their wild counterparts, elephants in zoos, circuses and sanctuaries are put in situations where they are required to adapt quickly to unnatural conditions. Taken out of their native environment, these animals are challenged by physiological and psychological factors that sometimes test the limits of their ability to cope and maintain a healthy state. The imbalance created by these factors may result in ill health or disease, and is not only a reflection of physiological stress, but also results in further suffering through the disease process itself. Elephant welfare is the responsibility not only of the elephants human caretakers but also of the society that has decided to keep elephants in their midst. Preventing disease and managing health problems humanely in our captive elephants is part of that responsibility. It is the premise of this chapter that, although good welfare may not guarantee good health, ill health and chronic disease indicate a lack of well-being and produce a state of diminished welfare. We postulate that objective measures of health and disease can be used as one of several indicators of well-being, and therefore recommend that routine monitoring of certain health parameters should be considered as one of the important tools used to assess general well-being and guide management decisions within captive elephant collections. What is disease and how does it relate to welfare? Disease can be defined as any impairment that interferes with or modifies the performance of normal functions, including responses to environmental factors such as nutrition, toxicants, climate, infectious agents, inherent or congenital defects or combinations of these factors (Wobeser 2006). Others have made a direct association between disease and suffering (Gregory 2004; Broom 2006). Disease states involve pathology, such as inflammation and destruction of tissues, which produce many physiological responses that result in well-recognized signs of suffering, such as pain, distress and depression, weakness, abnormal behavior, loss of appetite or starvation (Gregory 2004). If the disease is short-lived, consequences may be minimal. However, if the disease is chronic or
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repeated, it may result in permanent physiological outcomes such as structural defects, scars, arthritis, immune dysfunction or weakness that lead to further ill health and continued poor welfare. Health and disease represent a complex dynamic that is in constant flux. In most cases, disease-causing organisms such as parasites, bacteria and viruses are part of the normal ecology of an animal. Naturally occurring agents have evolved alongside or within the same environment as the host animal that has in turn evolved compensatory mechanisms to combat or control disease. The development of these compensatory mechanisms is called adaptation (Broom 2006). Some examples of compensatory or adaptive mechanisms are an effective immune system, detoxifying enzyme systems or behavioral adaptations that lead to avoidance of disease, trauma or predation. Adaptation occurs through a highly complex dynamic system that is governed by a myriad of internal and external factors. Internal or individual factors that may be important in the host include age, immune status, physical compromises secondary to trauma, physiological pressures (e.g., reproduction, growth, migration) and the nutritional status of that individual. Examples of important external factors would include social structure, and environmental factors such as climate, availability of water and food, and predation or introduction of novel agents. An animals ability or inability to adapt to changing internal and external challenges has direct consequences for well-being. In most cases, fluctuations or disturbances in internal and external factors are only temporary and will be compensated for through adaptive mechanisms designed to resolve imbalance. However, a disease state may persist or be so overwhelming as to overcome these adaptive mechanisms and result in compromise (i.e. illness or impairment), or even death. Very unusual circumstances, such as the extreme external challenges encountered in captivity, can push an animal past the threshold of its normal adaptive mechanisms, leading to a greater predisposition for disease and loss of well-being. One of the most significant responses to an internal and/or external imbalance that contributes to poor welfare is stress. Stress is a normal adaptive function and has some beneficial effects in the short term. However, chronic psychological or physiological stress, as may be experienced in association with chronic ill health, is detrimental, may result in immunosuppression and contributes to further disease (Gregory 2004; Broom 2006). As we discuss below and in the next chapter, many of the diseases of captive elephants are unique to their captive state and are likely to result, in part, from some level of chronic stress. What does it mean to be in captivity and how are humans involved? Elephants are influenced by human activities in multiple ways. In the optimal situation, wild animals living in the landscape in which they have evolved should be generally healthy and reproducing well (Lee & Moss, Chapter 2). Some would argue that no place on earth is free from human effects. One of the more extreme forms of human influences on elephants has been through the practice of capturing and maintaining them in captive settings. Elephants lend themselves to training and have been utilized by humans for thousands of years for work, worship and entertainment. However, any elephant living in captivity is still a wild animal. Because elephant reproduction in captivity has been so challenging, most captive elephants are only one or two generations removed from the wild and therefore have not undergone the selective breeding over multiple generations needed to successfully produce a domesticated animal (Sukumar 2003; Fowler & Mikota 2006). Thus, a trained elephant cannot be considered a domesticated elephant, and elephants in the captive context can be expected to be extraordinarily challenged both behaviorally and physiologically. As discussed above, animals placed in such conditions may reach the limits of their ability to
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adapt to these abnormal conditions and be prone to developing diseases or comprised health and therefore experience diminished welfare. Human society has a responsibility to minimize the negative impacts of keeping elephants in captivity, including the effective prevention and treatment of disease. This is especially compelling for diseases or conditions that develop in response to the captive environment. Elephant caretakers and veterinary professionals have the tools to investigate, treat, monitor and develop prevention strategies for minimizing diseases of captive elephants, contributing to our responsibility for their overall well-being. How can health assessments be used to monitor well-being? The presence or absence of disease in captive elephants can be both measured objectively and assessed quantitatively, making the evaluation of health status an especially useful tool in assessing the well-being of captive animals. Captive elephants in North America frequently exhibit a number of illnesses that are either not experienced at all by their wild counterparts, or not experienced at the same frequency. These diseases therefore create a lack of well-being in elephants that is a direct consequence of captivity. Many of these diseases are chronic in nature, and even though occasional illness due to accident or disease can be experienced by any animal, chronic disease states can certainly be equated to a lack of well-being. As veterinarians we are trained to focus on disease specifics: etiology, pathology and treatment options. Zoo veterinarians and others caring for captive elephants have developed many creative methods for assessing and treating our gargantuan patients, and great strides have been made in recent years in improving diagnostic modalities and medical treatments for elephants. While we are often charged with diagnosing and treating a sick elephant patient, frequently a more holistic investigation of the factors precipitating the particular disease state is not encouraged. Clearly defining and addressing the underlying factors contributing to the disease state are crucial to adequately improving the long-term well-being of these animals. Among these conditions are several infectious diseases, multiple husbandry-related conditions, nutritional diseases and reproductive dysfunction that all contribute to diminished welfare in the captive elephant. These impede elephants ability to effectively respond to new health challenges, thereby perpetuating further lack of well-being. How is captivity related to specific disease states? In captive elephant populations infectious diseases such as tuberculosis (Mikota, Chapter 6) and endotheliotropic elephant herpes virus (EEHV) infection can be directly related to transmission of organisms from one species to another unrelated species. Infection is directly related to the exposure of captive elephants to species with which they would not normally have direct contact in the wild. In the case of tuberculosis, the close proximity of captive elephants to humans creates an opportunity for exposure to the human M. tuberculosis organism that would be unlikely to occur in a wild elephant population. The many deaths of young captive elephants due to EEHV infection are thought to be related to the practice of mixing African and Asian elephants. This exposes Asian elephants to an organism that is carried relatively benignly by African elephants, but is fatal to Asian elephants (Fowler & Mikota 2006). Husbandry-related diseases such as foot problems, oral health problems and skin disease also have unique characteristics related to the captive setting. Pathological conditions of the elephant
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foot due to lack of mobility from inadequate space, development of stereotypic behaviors and inappropriate substrate are unique to captivity and frequently lead to euthanasia of captive elephants in North America. Dental problems seen in captivity can be precipitated by lack of appropriate browse material and inappropriate diets (see below; Fowler & Mikota 2006). Captivity in northern climates where indoor housing in heated barns is necessary for long periods of time creates the opportunity for pathological skin conditions not seen in the wild, as well as multiple other abnormal health conditions. Nutritional diseases are frequently encountered in captive elephants and range from inappropriately formulated diets to sand impaction colic. Hand raising infant elephants without complete knowledge of their nutritional requirements often results in young animals that fail to thrive (but see Sheldrick, Chapter 16; Fowler & Mikota 2006). Successful reproduction is often used as a measure of well-being in captive animals. Unfortunately, in captive elephant populations in North America, reproductive problems have been the norm rather than the exception. Due to the difficulties involved in providing opportunities for natural breeding, elephant reproduction is often only possible using artificial manipulation of the cow and bull. However, few institutions have the capacity to collect semen and many captive elephant cows have shown a variety of problems with cycling and lack the ability to conceive. Even if pregnancy is achieved, difficulties encountered during gestation and birth frequently result in loss of the calf. Raising calves to successful adulthood in which they are not only physically healthy but also retain the behavioral repertoire to function in a herd setting has also proven to be difficult in captivity. There are many challenges to the medical management of elephants in captivity. Captive settings for elephants range from zoos, circuses and sanctuaries, to working forestry elephants. The quality or quantity of veterinary care available in these settings varies widely but is not the sole determinant of animal health. An elephant at a spectacular and well-funded zoo facility with access to top-quality medical care may still experience a more compromised state of well-being overall than the forestry elephant. The captive setting as a whole will be directly reflected in the health and well-being of the elephant in that setting. There are excellent resources available to guide monitoring of captive elephant health, especially the Guidelines for Comprehensive Elephant Health Monitoring Program (American Zoo and Aquarium Association 2005). This type of resource provides a framework for the routine and careful monitoring of specific health parameters. These data need to be utilized in an ongoing strategy for assessment and improvement of well-being in a collection. It is important to build creative communication forums and networks that promote the value of sharing information and conducting cooperative research endeavors, leading to the improved health and well-being of captive elephants. Thorough health monitoring is only the first step in assessing the well-being of a captive elephant. The information gathered must then be analyzed and any factors underlying the health issues must be carefully evaluated. A commitment to addressing these underlying factors, however difficult that may prove to be, must be present at all levels in order for us to fully accept the responsibility for improving the health and well-being of the captive elephants in our care todayand in the future.

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American Zoo and Aquarium Association. 2005. Guidelines for comprehensive elephant health monitoring program. Elephant Species Survival Plan, http://www.elephantcare.org/protodoc_files/2005/Eleph% 20SSP%20Routine%20Health%20May%202005.pdf Broom DM. 2006. Adaptation. Berl Munch Tierarztl Wochenschr. 119(1-2):1-6. Fowler ME, Mikota SK. 2006. Biology, medicine and surgery of elephants. Ames, IA: Blackwell Publishing. Gregory NG. 2004. Physiology and behaviour of animal suffering. Ames, IA: Blackwell Publishing. Sukumar R. 2003. The living elephants: evolutionary ecology, behavior, and conservation. New York, NY: Oxford University Press. Wobeser GA. 2006. Essentials of disease in wild animals. Ames, IA: Blackwell Publishing.

References

Gretchen Kaufman is an Assistant Professor of Veterinary Medicine in the Department of Environmental and Population Health and Director of the Tufts Center for Conservation Medicine. She graduated from Tufts University School of Veterinary Medicine and completed a residency in zoological medicine at the University of California, Davis. She went back to Tufts to create and run the Exotic Animal Medicine Service in the small animal teaching hospital. After six years she returned to the Tufts Wildlife Clinic where she has continued clinical teaching, clinical and international research and didactic teaching in zoo, wildlife and exotic companion animal medicine. Dr. Kaufman focuses on wildlife medicine curriculum development in the veterinary program, spearheading graduate programs in conservation medicine and coordinating environmental education at the Tufts Institute for the Environment. She conducts veterinary medical research and service projects in Nepal, primarily on rabies prevention/ control and the dynamics of tuberculosis among humans, domestic animals and wildlife (including elephants). Dr. Kaufman also chairs the Greening the Grafton Campus Committee, working with other members of the campus community to reduce the environmental footprint of all aspects of the veterinary schools activities. She may be reached at Cummings School of Veterinary Medicine, Tufts University, 200 Westboro Road, North Grafton, MA 01536 or gretchen.kaufman@tufts.edu. Janet Martin obtained her DVM degree from the Tufts University School of Veterinary Medicine in 1990. After completing two internships, one in Small Animal Surgery and one in Wildlife and Zoo Medicine, she joined the staff of Roger Williams Park Zoo as the Associate Veterinarian. In 1997 after a six-month sabbatical at the Royal Melbourne Zoo in Australia, she returned to Roger Williams Park Zoo as the Director of Veterinary Services. Dr. Martin acts as the veterinary advisor to both the Monotreme and Marsupial Taxon Advisory Group of the American Association of Zoos and Aquariums, and the Tree Kangaroo Conservation Project, and in 1999 and 2003 accompanied the TKCP field research team to Papua New Guinea. Dr. Martin is currently a Research Assistant Professor at Tufts University Cummings School of Veterinary Medicine working on infectious disease in wildlife. She may be contacted at Cummings School of Veterinary Medicine, Tufts University, 200 Westboro Road, North Grafton, MA 01536 or janet.martin@tufts.edu.

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Chapter 6 Stress, Disease and Tuberculosis in Elephants


Susan K. Mikota Director of Veterinary Programs and Research Elephant Care International Tuberculosis (TB) is one of the most serious diseases affecting captive elephants today. It also has potentially grave consequences for wild populations. Although animals are the source of many human diseases, it appears that humans are most often the source of TB for elephants. The interrelationship between stress and disease is now widely acknowledged in human and veterinary medicine. Can this information benefit elephants? What do we know about TB in elephants? Is further research needed? Can information about stress and TB in humans be of value for infected elephants? Can we prevent the introduction of this devastating disease to the wild before it affects this endangered species as it has affected our own species? An understanding of TB in humans will lay the groundwork for a clearer understanding of TB in elephants. I will discuss TB and stress in humans and then present a brief history of TB in elephants and the challenges to diagnosis and treatment in our largest land mammal. I will explore the implications of stress in the pathogenesis of TB in elephants. I will voice concerns for the potential introduction of TB into wild elephant populations and conclude with a discussion of current and future research. Tuberculosis: a global crisis In an age when the human immunodeficiency virus (HIV), Ebola virus, cancer and heart disease command the health news headlines, TB is an often-forgotten disease. Yet, worldwide, it is the leading cause of death from an infectious agent. Thirty million people died from TB in the decade between 1995 and 2005. A startling two billion peopleone-third of the earths population are currently infected. TB is endemic in Southeast Asia and 33 percent of all cases occur in this region. The highest mortality, however, occurs in Africa due to co-infection with HIV and a lack of resources for surveillance and drugs for treatment. Tuberculosis has been reported in every state in the United States and between 10 and 15 million Americans are infected. One observer describes TB as Ebola with wings to depict the ease with which it has spread across the globe. The World Health Organization (WHO) has designated TB a global crisis, and a major initiative, The Global Plan to Stop TB 2006-2015, aims to cut human TB deaths in half by 2015 compared to 1990 levels (See the Stop TB Partnership http://www.stoptb.org/globalplan/ for more information).

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What causes TB? Tuberculosis is caused by a bacterium discovered by Robert Koch in 1882. Unlike most bacterial diseases that run their course quickly, TB is an insidious and chronic disease that may linger for decades or remain hidden only to explode into an acute crisis. The causative agent in humans is Mycobacterium tuberculosis, a member of the Mycobacterium tuberculosis complex. Other members and their target species include M. bovis (cattle), M. africanum (the human form in Africa), M. microti (voles) and M. bovis BCG (the strain used to make vaccines).There are over 100 other species of mycobacteria, including an avian form (M. avium) and numerous non-tuberculous forms that are found commonly in the environment. These are also known as MOTT (mycobacteria other than tuberculous). Mycobacteria can infect humans, non-human primates, domestic and wild ungulates and carnivores, marine mammals, psittacine birds, reptiles and fish. Susceptibility to specific mycobacteria varies with the species (Montali, Mikota & Cheng 2001). The human form of TB occasionally infects dogs and parrots and has even been diagnosed in cattle and bongo antelope. Humans are susceptible to the bovine form of TB and immuno-compromised individuals may become infected with avian TB. The discovery that bovine TB was transmitted to humans via cows milk precipitated legislation requiring the pasteurization of milk and cheese. Tuberculosis in elephants in the United States is caused primarily by the human strain, although one case due to M. bovis has been reported and an unusual non-tuberculous mycobacteria has affected two elephants (Lacasse, Terio, Kinsel, Farina et al. 2007). Tuberculosis due to M. bovis may be more common in Asian range countries where captive elephants share grazing land with domestic cattle. How is TB transmitted? TB is transmitted by aerosolization. Infective droplets may be released into the air when an infected person speaks, coughs or sneezes. Tuberculosis can only be transmitted from individuals with active infections. A number of factors influence the probability that an individual will become infected after an exposure. The virulence of the organism, the infectiousness of the carrier, the environment in which the exposure occurred and the duration of the exposure all come into play. A casual exposure is less likely to result in infection than a chronic exposure. Health care workers are therefore at greater risk. Many TB cases are clustered in households because there are multiple opportunities for infection to be transmitted among family members. A single concentrated exposure may also result in infection (Dalovisio, Montenegro-James, Kemmerly, Genre et al. 1996). How is TB diagnosed in humans? The intradermal tuberculin test (also known as the Mantoux test) is used in humans as a screening test for TB. A small amount of tuberculin is injected intradermally (within the skin). Tuberculin is a diagnostic agent derived from particular strains of bovine TB (bovine strains are used because bovine and human TB are very closely related and will cross-react). The test is read at 48 hours by observing the injection site for evidence of induration (swelling). The measurement of the induration, together with the individuals risk category, determine whether the test is positive. A 15-mm swelling is considered positive in almost all cases. A 10-mm reaction is positive in drug users and in recent arrivals from certain high-TB-risk countries. A five-mm reaction is positive in individuals who are immuno-compromised (from chemotherapy or HIV, for example) or if there has been a recent contact with a known active TB case.
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After exposure to TB, there are five possible scenarios: 1) no infection occurs; 2) infection is established and there is acute disease; 3) infection is established but later eradicated; 4) infection is established and containedthis is latent disease; or 5) infection is established, contained and then reactivated. In all but the first scenario, a human will have a positive tuberculin test. Following a positive skin test, further diagnostics such as sputum cultures and chest radiographs are employed to determine whether active disease is present. According to the WHO, latently infected humans with normal immune systems have a four to 10 percent chance of developing active TB at some point in their lives. Immunodeficiency disorders such as HIV present a significant risk factor for the development of active TB. Further information about TB in humans is available from the Centers for Disease Control (http://www.cdc.gov/nchstp/tb/default.htm). Stress and TB in humans While the association between stress and disease has been noted as far back in time as Aristotle (fourth century BCE), it is only recently, through the development of the field of psychoneuroimmunology, that a scientific basis for this association has been elucidated. Stress and the underlying neuro-endocrine mechanisms that define the stress response were discussed in detail by Bradshaw (Chapter 4). Numerous factors affect how an individual animal will respond to stress. These include species differences, individual differences, sex, age, reproductive stage, social position and prenatal, neonatal or early experiences. Animal studies have shown that susceptibility to disease may increase, decrease or remain unchanged depending on the speciesstressor-pathogen combination. Chronic stress (distress) suppresses the immune system, diminishes wound healing and decreases the inflammatory response. Glucocorticoids decrease circulating lymphocytes (B cells, T cells and Natural Killer cells) that modulate the response to invading pathogens. The central nervous system, which has a direct effect on the organs where lymphocytes are produced and stored (the bone marrow, thymus, spleen and lymph nodes), is also involved. These pathways are complex and a detailed discussion is beyond the scope of this chapter. Simply stated, the status of the immune system determines how a human (or an elephant) will respond after a TB exposure and stress can profoundly influence the immune system. Social deprivation has been shown to affect immunity and long-term survival in monkeys (Lewis, Gluck, Petitto, Hensley et al. 2000) and it is reasonable to expect that this may also be true for elephants. Many elephants in captivity were wild-caught as youngsters and separated from their mothers and families. African elephants in particular likely witnessed the slaughter of related adults during the capture process (Bradshaw, Chapter 4; Lee & Moss, Chapter 2; Poole & Granli, Chapter 1; Sheldrick, Chapter 16). These young elephants were weaned prematurely and transported to live in conditions drastically different from those to which they are ecologically and evolutionarily adapted. Movement of elephants between facilities was (and to an extent still is) a common practice, thus further preventing or disrupting social bonds critical to elephant well-being. While the effects of these early stressors on the elephant immune system and survivability have not been studied, it would be interesting to do so, and to compare the life histories of elephants that become infected following exposure to TB, with those that do not. The association between stress and TB was presented to the scientific community in a landmark study The Influence of Psychic Acts on the Progress of Pulmonary Tuberculosis, published in 1919. The author, Thoru Ishigami, reported that he and numerous other colleagues had observed that the mental state of their patients significantly influenced the course of TB progression. Nervous patients or those experiencing financial or personal loss were more likely to succumb to TB
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than optimistic patients with few worries (Ishigami 1919). Ishigami also demonstrated that adrenaline (i.e. stress) inhibited the phagocytosis (engulfing) of M. tuberculosis by macrophages in vitro. Ishigami suggested that the high rate of TB among Japanese students was due to the inherent stress of the educational system in place at the time. His appeal for educational reform went unheeded. The bodys defense systems determine the outcome of events following exposure to TB. One person may avoid infection altogether and another develop overwhelming disease. It all depends on the individuals immune response. In 1956, Hans Selye, the father of the General Adaptation Syndrome (the stress response) suggested that these varying responses to TB might be mediated via adreno-cortical-tropic hormone (ACTH) and cortisol. Selye did not think that stress directly caused disease. Rather he believed that the bodys capacity to resist disease and overcome the stress component often meant the difference between succumbing and not succumbing to a disease (Selye 1956). Rats are naturally resistant to TB and will not become infected even when injected with the organism. Rats injected with TB and ACTH, however, not only become infected; they die. Under the influence of ACTH (mimicking stress), their innate genetic resistance to TB is overcome. Of this experiment, conducted in 1952, Selye commented: This experiment gives food for thought and raises the question: What is disease due to? It shakes our certainty in the pathogenesis of disease being due to any one particular agent. It makes us think rather that many diseases are due to pathogenic situations, to a constellation of disease-producing circumstances, all of which must be present at the time in order to cause the disease. (Selye 1956, p. 60-61) While it appears that stress can overcome the inherent resistance of a species, genetics is another determinant of individual resistance or susceptibility to TB. Genetic epidemiology is an active area of TB research in humans (Kim, Lee, Lee, Sin et al. 2003; Liu, Cao, Zhang, Tian et al. 2004; Malik, Abel, Tooker, Poon et al. 2005; Barreiro, Neyrolles, Babb, Tailleux et al. 2006; Li, Zhang, Zhou, Huang et al. 2006). Genetic differences may explain why dexamethasone (a steroid drug that induces the same changes in the body as a stress response) administration will increase the growth of TB in blood monocyte cells from some donors but will have no effect on TB growth in monocytes from other donors (Boomershine & Zwilling 2000). While we owe a debt of gratitude to Louis Pasteur and Robert Koch for advancing our knowledge of pathogens and disease, the germ theory has left a legacy that suggests that microorganisms are the sole perpetrators of disease, when indeed they are but one factor in the complex constellation that Selye described. Even Pasteur on his deathbed said, Le germe nest rien, cest le terrain qui est tout (The microbe is nothing, the soil is everything, as quoted in Selye 1956, p. 59). T. H. Holmes studied patients at a TB sanatorium and demonstrated a positive correlation between TB and stressful events that occurred years prior to the disease. His later studies also showed higher rates of recidivism, compared to controls, among patients who experienced emotional problems while hospitalized (Holmes 1956). Prior to the discovery of antibiotics, TB was treated with rest, fresh air, sunshine and good nutrition and many patients improved. The home sanatorium method of Joseph Hersey Pratt utilized these basic therapies but added class meetings (a forerunner of group therapy) and a friendly visitor (todays social worker or public health nurse). That Pratt achieved better results than two
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traditional sanatoriums is likely due to the stress-reducing effects of the social support that is now accepted as a component in the treatment of many diseases (Sabin 1990). The bodys immune response to TB is complex and has not yet been thoroughly explained. Recent research is helping to explain why some of the treatments employed prior to the availability of antibiotics were effective. We know that the TB organism is killed by sunlight. A team of researchers at the University of California, Los Angeles (UCLA) and the Harvard School of Public Health has recently demonstrated that vitamin D plays a crucial role in the production of cathelicidin, which kills TB bacteria. Vitamin D is produced by the body when sunlight reaches the skin; however, the skin pigment melanin, more abundant in darker skin, shields the body from the suns rays and reduces vitamin D production. This finding explains why people of African descent are more susceptible to TB than Caucasians and have more severe disease. It also explains why sanatoriums in sunny mountain locations were an effective traditional treatment (Liu, Stenger, Li, Wenzel et al. 2006). A brief history of TB in elephants TB has plagued both man and animal since ancient times. Tuberculous scarring has been observed on the bones of mastodon skeletons recovered in North America and dating to the last ice age (Rothschild & Laub 2006), and DNA from the human form of TB has been isolated from a 17,000-year-old bison bone (Hecht 2001). The first evidence that elephants might contract tuberculosis derives from Sanskrit documents over 2,000 years old (Iyer 1937). While the causative organism was obviously unknown at this time, the disease was described clearly. In more recent times, a case at the London zoo in 1875 (Garrod 1875) was followed by sporadic reports in the early and mid-1900s (Damman 1909; Thieringer 1911; Narayanan 1925; Bopayya 1928; Baldrey 1930; Gorovitz 1962; Seneviratna, Wettimuny & Seneviratna 1966; Gorovitz 1969; Pinto, Jainudeen & Panabokke 1973; Greenberg, Jung & Gutter 1981; Gutter 1981; Jones & Good 1982; Saunders 1983). African elephants are susceptible to TB (Gorovitz 1962, 1969), but most cases have occurred in Asian elephants. Whether or not this reflects a greater susceptibility to TB among Asian elephants is unknown. Asian elephants have been maintained in captivity for over 2,000 years, a history that is not shared by African elephants. The seemingly greater susceptibility of Asian elephants to TB may simply reflect their closer relationship and exposure to TB-infected humans. The year 1996 is often regarded as the year that elephant TB emerged in the United States. The highly publicized deaths of two circus elephants from advanced TB within a three-day period prompted concern from both the public and the United States Department of Agriculture (USDA). Other cases were soon to follow in the United States (Binkley 1997; Mikota, Larsen & Montali 2000; Mikota, Peddie, Peddie, Isaza et al. 2001) and Europe (Gavier-Widen, Hard Af Segerstad, Roken, Moller et al. 2002; Lewerin, Olsson, Eld, Roken et al. 2005; Moller, Roken, Petersson, Vitaud et al. 2005). The circus elephant deaths led to the formation of an Elephant TB Advisory Panel and subsequently to the National Tuberculosis Working Group for Zoo and Wildlife Species. These groups were charged with the task of developing strategies to diagnose and control the disease in elephants and non-domestic ungulates. What resulted in 1998 was a document entitled Guidelines for the Control of Tuberculosis in Elephants that specifies methods for diagnosis, surveillance and treatment. It is administered by the USDA as Policy 21 under the Animal Welfare Act. The Guidelines were revised in 2000, 2003 and 2007 (in progress) as research led to a better understanding of TB
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in elephants (USDA 2003). How is TB diagnosed in elephants? Determining whether an elephant has active TB can present a diagnostic challenge. Many elephants do not show clinical signs until the disease is quite advanced. Radiography is not feasible in elephants as x-rays cannot penetrate their large mass. The intradermal tuberculin test is not accurate in elephants (Mikota et al. 2001; Lewerin et al. 2005). What has evolved as the gold standard test is the trunk washthe elephant equivalent of a sputum culture. The sample is collected by training elephants to accept the instillation of sterile saline into their trunks. The saline washes the lining of the trunk and serves as a vehicle to collect any pathogenic organisms that may be present. Elephants are taught to exhale into a zip-lock bag that serves as a collection device, and then the sample is transferred to a secure tube, and submitted to a laboratory for culture. From this point on, the lab procedures are the same for elephants as for humans. While culture is the current gold standard, it has inherent limitations. Similar to humans, elephants can shed TB intermittently so a triple sample method is used (three samples collected on separate days over the course of a week) to increase the chances of detection. Although a positive culture is diagnostic for TB, a negative culture does not necessarily rule out disease, because an infected animal may not have been shedding at the time of sample collection. Experimental serological tests have shown great promise to diagnose TB in elephants (Larsen, Salman, Mikota, Isaza et al. 2000; Lyashchenko, Singh, Colangeli & Gennaro 2000; Anon 2005; Lyashchenko, Miller & Waters 2005; Lyashchenko, Greenwald, Esfandiari, Olsen et al. 2006). In some cases, these tests have been positive years in advance of culture. Serological tests are indirect that is, they detect antibodies to TB rather than detecting the actual TB organism. Is TB in elephants a health risk for humans? Tuberculosis is a zoonotic disease and can potentially be transmitted from animals to humans. In the only published report of an elephant and human infected with the same TB strain, it could not be proven whether the transmission was from elephant to human or human to elephant (Michalak, Austin, Diesel, Bacon et al. 1998). While many variables determine the course of events following exposure to TB, the duration of exposure is one of the most significant, thus placing elephant handlers and veterinarians at greatest risk (Davis 2001; Oh, Granich, Scott, Sun et al. 2002). While contracting TB from an elephant during a casual exposure is possible, it is not likely in healthy humans with functional immune systems. How is TB in elephants treated? Ironically, while animals are typically the model for human diseases, in the case of TB, humans are the model for elephants. This has occurred for two reasons. First, there is no acceptable animal model upon which to base our approach to TB in elephants. Tuberculosis in cattle is controlled by a test and slaughter program that cannot be applied to animals like elephants. There is very little information available on TB treatment in cattle or any other animal species. Secondly, as elephants are affected primarily by the human form of TB, it is logical to apply to elephants what is known about the disease in humans. The treatment protocols that are a part of the Guidelines for the Control of Tuberculosis in Elephants are therefore based on protocols used for humans. The same drugs are used, although elephants are generally treated for a longer period. This is to provide for a greater margin of safety while we continue to study the pathogenesis of TB in elephants. Studies that we have conducted
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in elephants to measure blood levels of anti-tuberculosis drugs have supported this approach and we can achieve drug levels in elephants known to be effective (i.e. curative) in humans (Maslow, Mikota, Zhu, Isaza et al. 2005; Maslow, Mikota, Zhu, Riddle et al. 2005; Zhu, Maslow, Mikota, Isaza et al. 2005; Peloquin, Maslow, Mikota, Forrest et al. 2006). Depending on the drug, it may be administered orally or rectally. Elephants have an exquisite sense of taste and will often reject oral medications, even if hidden in the tastiest of treats. Conversely, they can be readily conditioned to accept rectal administration and this route is preferred for the anti-tuberculosis drugs isoniazid and pyrazinamide. Rifampin, one of the main drugs, can only be given orally however, as adequate blood levels cannot be achieved with rectal administration. Like humans, elephants may experience drug side effects such as appetite loss and elevation of liver enzymes from some of the anti-tuberculosis drugs. Careful monitoring is required during treatment. Stress and TB in elephants There is much that we do not yet know about TB in elephants. As of this writing, about 12 percent of Asian elephants in the United States were diagnosed with TB between 1994 and 2006. It is likely that this is an underestimation of the true number of infected elephants, as TB can remain latent for years. The serological tests discussed above have predicted the onset of disease years in advance of positive cultures and it is likely that more infected elephants will be identified once these tests become more widely available. Are elephants as a species more susceptible to TB? Other species kept in captivity in close association with people (tigers in circuses, for example) have not become infected. Genetics is a primary determinant of disease susceptibility of resistance in humans. Do elephants carry genes that confer susceptibility of resistance to TB? A pilot study to investigate this is about to begin (see http://www.elephantcare.org). What about Vitamin D? Perhaps the dark skin of the elephant also affects Vitamin D production and cathelicidin as described in the human study above. It would be interesting to investigate this possibility. It is widely accepted that stress influences both susceptibility to TB and its severity once infection is established (Boomershine 2000). Given the clear association between stress and TB in humans it is logical to assume a similar association between stress and TB in elephants (and perhaps other diseases as well). The numerous stressors experienced by captive elephants have been described adequately above and in other chapters of this book. Recall that TB is a human disease and that elephants in captivity are exposed to a disease they would not normally encounter living in their natural habitat in the wild. Although prompt identification of infected individuals, initiation and completion of appropriate therapy and ongoing surveillance of the population are critical to the control of TB in elephants, the role of stress should not be overlooked. Differences (or variations) in husbandry, nutrition and social well-being may influence which elephants succumb to disease following exposure, and which elephantsonce infectedrespond to treatment. The occurrence of TB in elephants may be a symptom of a greater problemnamely our inability to meet the social and biological needs of this amazing and intelligent animal. Implications for wild elephant populations Tuberculosis has not yet been reported in wild elephants. There is undoubtedly the potential for this occurrence and the absence of reports may only reflect a lack of surveillance. Tuberculosis has been reported in the literature and anecdotally in captive elephants in several of the 13 Asian
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range countries (where elephants are still found in the wild). These are the same countries where TB is highly endemic within the human population. The elephant is revered in many parts of Asia and is both a cultural and religious icon. Elephants are common at temples, festivals and tourist attractions in India, Nepal and Thailand. These events present ample opportunity for elephant-human intermingling and the spread of disease between species. Although TB in elephants probably originated from humans, infected elephants may be a potential reservoir to pass the disease back to humans. This epidemiological possibility is yet to be explored. In some countries it is common for wild and captive elephants to intermingle. Captive elephants may be released into the forest to browse at night or wild bulls may enter camps to breed receptive elephant cows. Such management practices pose a great risk for disease transfer to wild elephants. The transfer of a primary human pathogen into free-ranging wildlife has already occurred with the introduction of M. tb to free-ranging banded mongooses (Mungos mungo) in Botswana and suricates (Suricata suricatta) in South Africa (Alexander, Pleydell, Williams, Lane et al. 2002), suggesting that free-ranging African elephants, as well as Asian, may be at risk. The potential for the introduction of TB into wild elephant populations is of great concern. Prevention is crucialif it is not already too late. Research needs Elephant tuberculosis research is ongoing and is a major focus of Elephant Care International (http://www.elephantcare.org/projects.htm#Initiative). Additional studies are needed to identify alternative therapeutic agents that minimize some of the side effects that have been observed. More cost-effective treatments must be identified if captive elephants in Asia are to be treated. The cost of treating a single elephant in the United States exceeds $50,000. The new serological tests promise improved means of diagnosis, but still lacking is a rapid diagnostic test to identify elephants that are shedding the bacteria. Currently under investigation in both humans and elephants is a biosensora breathalyzer that detects the Mycobacterium tuberculosis organism instantly. Improved diagnostics like the above, and others as yet undeveloped, will be critical to the management of elephants in Asia where segregation may be an alternative to costly treatment to prevent the spread of disease to other elephants or humans. If the genetic study described above reveals that elephants have a gene that confers susceptibility (or resistance) to TB, this too could be used as a management tool to limit exposure of elephants at risk and prevent TB introduction to already threatened wild populations. References

Alexander KA, Pleydell E, Williams MC, Lane EP, Nyange JFC, Michel AL. 2002. Mycobacterium tuberculosis: an emerging disease of free-ranging wildlife. Emer Infect Dis 8:598-601. Anon. 2005. Summary elephant tuberculosis research workshop. http://www.elephantcare.org/protodoc_ files/2005/Elephant%20Tuberculosis%20 Research%20Workshop%20May%2005.pdf Baldrey FSH. 1930. Tuberculosis in an elephant. J R Army Vet Corp 1:252. Barreiro LB, Neyrolles O, Babb CL, Tailleux L, Quach H, McElreavey K, van Helden PD, Hoal EG, Gicquel B, Quintana-Murci L. 2006. Promoter variation in the DCSIGN-encoding gene CD209 is associated with tuberculosis. PLoS Med 3(2):e20. Binkley M. 1997. Tuberculosis in captive elephants. Proc AAZV. p. 116-119.

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Boomershine CS, Zwilling BS. 2000. Stress and the pathogenesis of tuberculosis. Clin Microbiol News 22:177-182. Bopayya AB. 1928. Tuberculosis in an elephant. Indian Vet J 5:142-145. Dalovisio JR, Montenegro-James S, Kemmerly SA, Genre CF, Chambers R, Pankey GA, Failla DM, Haydel KG, Hutchinson L, Lindley MF, Praba A, Eisenach KD, Cooper ES. 1996. Comparison of the amplified Mycobacterium tuberculosis (MTB) direct test, aplicor MTB PCR and IS6, 110-PCR for detection of MTB in respiratory specimens. Clin Infect Dis 23:1099-1106. Damman S. 1909. Tuberculosis diseases in elephants with human type Mycobacterium. Deutsche Tierarztl Wschr 17:345. Davis M. 2001. Mycobacterium tuberculosis risk for elephant handlers and veterinarians. Appl Occup Environ Hyg 16:350-353. Garrod AH. 1875. Report on the Indian elephant which died in the societys gardens on July 7th, 1875. Proc of the Zool Soc of London 1875:542-543. Gavier-Widen D, Hard Af Segerstad C, Roken B, Moller T, Bolske G, Sternberg S. 2002. Mycobacterium tuberculosis infection in Asian elephants (Elephas maximus) in Sweden. Paper presented at the European Association of Zoo and Wildlife Veterinarians 4th Scientific Meeting, Heidelberg, Germany. Gorovitz C. 1962. Tuberculosis in an African elephant. Nord Vet Med 14:351-352. Gorovitz C. 1969. Tuberculosis in an African elephant. Am Assoc of Zoo Vet News January 20. Greenberg HB, Jung RC, Gutter AE. 1981. Hazel elephant is dead (of tuberculosis) (letter). Am Rev Respir Dis 124:341. Gutter A. 1981. Mycobacterium tuberculosis in an Asian elephant. Proc AAZV. p. 105-106. Hecht J. 2001. Telltale bones. New Scientist 2312:14. Holmes TH. 1956. Multidiscipline studies of tuberculosis. In: Sparer PJ, ed. Personality, stress, and tuberculosis. New York, NY: Int Univ Press. p. 65-125. Ishigami T. 1919. The influence of psychic acts on the progress of pulmonary tuberculosis. Am Rev Tuberc 2:470-484. Iyer AK. 1937. Veterinary science in India, ancient and modern with special reference to tuberculosis. Agric Livest India 7:718-724. Jones WD, Jr., Good RC. 1982. Hazel elephant redux (letter). Am Rev Respir Dis 125:270. Kim JH, Lee SY, Lee SH, Sin C, Shim JJ, In KH, Yoo SH, Kang KH. 2003. NRAMP1 genetic polymorphisms as a risk factor of tuberculous pleurisy. Int J Tuberc Lung Dis 7(4):370-375. Lacasse C, Terio K, Kinsel MJ, Farina LL, Travis DA, Greenwald R, Lyaschenko KP, Miller M, Gamble K. 2007. Two cases of atypical mycobacteriosis caused by Mycobacterium szulgai associated with mortality in captive African elephants (Loxodonta africana). J Zoo Wildl Med 38:101-107. Larsen RS, Salman MD, Mikota SK, Isaza R, Montali RJ, Triantis J. 2000. Evaluation of a multiple-antigen enzyme-linked immunosorbent assay for detection of Mycobacterium tuberculosis infection in captive elephants. J Zoo Wildl Med 31:291-302. Lewerin SS, Olsson SL, Eld K, Roken B, Ghebremichael S, Koivula T, Kallenius G, Bolske G. 2005. Outbreak of Mycobacterium tuberculosis infection among captive Asian elephants in a Swedish zoo. Vet Rec 156:171-175. Lewis MH, Gluck JP, Petitto JM, Hensley LL, Ozer H. 2000. Early social deprivation in nonhuman primates: long-term effects on survival and cell-mediated immunity. Soc of Biolog Psychiatry 47:119-126. Li HT, Zhang TT, Zhou YQ, Huang QH, Huang J. 2006. SLC11A1 (formerly NRAMP1) gene polymorphisms and tuberculosis susceptibility: a meta-analysis. Int J Tuberc Lung Dis 10(1):3-12. Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Krutzik S, Ochoa MT, Schauber J, Wu K, Meinken C, Kamen DL, Wagner M, Bals R, Steinmeyer A, Zugel U, Gallo RL, Eisenberg D, Hewison M, Hollis BW, Adams JS, Bloom BR, Modin RL. 2006. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Electronic Citation 10.1126/science.1123933.

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Liu W, Cao WC, Zhang CY, Tian L, Wu XM, Habbema JDF, Zhao QM, Zhang PH, Xin ZT, Li CZ, Yang H. 2004. VDR and NRAMP1 gene polymorphisms in susceptibility to pulmonary tuberculosis among the Chinese Han population: a case-control study. Int J Tuberc Lung Dis 8(4):428-434. Lyashchenko KP, Greenwald R, Esfandiari J, Olsen JH, Ball R, Dumonceaux G, Dunker F, Buckley C, Richard M, Murray S, Payeur JB, Andersen P, Pollock JM, Mikota S, Miller M, Sofranko D, Waters WR. 2006. Tuberculosis in elephants: antibody responses to defined antigens of Mycobacterium tuberculosis, potential for early diagnosis, and monitoring of treatment. Clin Vaccine Immunol 13:722-732. Lyashchenko K, Miller M, Waters WR. 2005. Application of MAPIA (Multiple antigen print immunoassay) and rapid lateral flow technology for tuberculosis testing of elephants. Proc AAZV, AAWV, AZA Nutrition Advis Grp. p 64-65. Lyashchenko K, Singh M, Colangeli R, Gennaro ML. 2000. A multi-antigen print immunoassay for the development of serological diagnosis of infectious disease. J Immunol Meth 242:91-100. Malik S, Abel L, Tooker H, Poon A, Simkin L, Girard M, Adams GJ, Starke JR, Smith KC, Graviss EA, Musser JM, Schurr E. 2005. Alleles of the NRAMP1 gene are risk factors for pediatric tuberculosis disease. PNAS 102(34):12183-12188. Maslow JN, Mikota SK, Zhu M, Isaza R, Peddie LR, Dunker F, Peddie J, Riddle H, Peloquin CA. 2005. Population pharmacokinetics of isoniazid in the treatment of Mycobacterium tuberculosis among Asian and African elephants (Elephas maximus and Loxodonta africana). J Vet Pharmacol Ther 28:1-7. Maslow JN, Mikota SK, Zhu M, Riddle H, Peloquin CA. 2005. Pharmacokinetics of ethambutol (EMB) in elephants. J Vet Pharmacol Ther 28:321-323. Michalak K, Austin C, Diesel S, Bacon MJ, Zimmerman P, Maslow JN. 1998. Mycobacterium tuberculosis infection as a zoonotic disease: transmission between humans and elephants. Emerg Infect Dis 4:283287. Mikota SK, Larsen RS, Montali RJ. 2000. Tuberculosis in elephants in North America. Zoo Biol 19:393403. Mikota SK, Peddie L, Peddie J, Isaza R, Dunker F, West G, Lindsay W, Larsen RS, Salman MD, Chatterjee D, Payeur J, Whipple D, Thoen C, Davis DS, Sedgwick C, Montali R, Ziccardi M, Maslow J. 2001. Epidemiology and diagnosis of Mycobacterium tuberculosis in captive Asian elephants (Elephas maximus). J Zoo Wildl Med 32:1-16. Moller T, Roken B, Petersson L, Vitaud C, Lyashchenko K. 2005. Preliminary results of a new serological test for detection of TB infection (Mycobacterium tuberculosis) in elephants (Elephas maximus and Loxodonta africana) - Swedish Case studies. Verh ber Erkrg Zootiere. p. 173-181. Montali RJ, Mikota SK, Cheng LI. 2001. Mycobacterium tuberculosis in zoo and wildlife species. Revue Scientif et Techni Office International des Epizooties 20:291-303. Narayanan RS. 1925. A case of tuberculosis in an elephant. J Comp Pathol 38:96-97. Oh P, Granich R, Scott J, Sun B, Joseph M, Stringfield C, Thisdell S, Staley J, Workman-Malcolm D, Borenstein L, Lehnkering E, Ryan P, Soukup J, Nitta A, Flood J. 2002. Human exposure following Mycobacterium tuberculosis infection of multiple animal species in a metropolitan zoo. Emerg Infect Dis 8:1290-1293. Peloquin CA, Maslow JN, Mikota SK, Forrest A, Dunker F, Isaza R, Peddie LR, Peddie J, Zhu M. 2006. Dose selection and pharmacokinetics of rifampin in elephants for the treatment of tuberculosis. J Vet Pharmacol Ther 29:1-6. Pinto MRM, Jainudeen MR, Panabokke RG. 1973. Tuberculosis in a domesticated Asiatic elephant Elephas maximus. Vet Rec 93:662-664. Rothschild BM, Laub R. 2006. Hyperdisease in the late Pleistocene: validation of an early 20th century hypothesis. Naturwissenschaften 93(11):557-564. Sabin JE. 1990. Joseph Hersey Pratts cost-effective class method and its contemporary application. Psychiatry 53:169-184. Saunders G. 1983. Pulmonary Mycobacterium tuberculosis infection in a circus elephant. JAVMA 183:13111312. 83

Selye H. 1956. Recent progress in stress research, with reference to tuberculosis. In: Sparer PJ, ed. Personality, stress, and tuberculosis. New York, NY: Int Univ Press. p. 45-64. Seneviratna P, Wettimuny SG, Seneviratna D. 1966. Fatal tuberculosis pneumonia in an elephant. Vet Med Small Anim Clinician 60:129-132. Thieringer H. 1911. About tuberculosis in an elephant. Berl Tierarztl Wschr 27:234-235. USDA 2003. Guidelines for the control of tuberculosis in elephants. http://www.aphis.usda.gov/ ac/TBGuidelines2003.pdf or http://www.elephantcare.org/protodoc_files/new2004/TB%20 Guidelines%202003%20Final.pdf. Zhu M, Maslow JN, Mikota SK, Isaza R, Dunker F, Peloquin CA. 2005. Population pharmacokinetics of pyrazinamide in elephants. J of Vet Pharmac & Therap 28:403-409.

Susan Mikota, DVM, has been actively engaged in elephant care, research and conservation for 15 years. Dr. Mikota is a co-founder of Elephant Care International (http://www.elephantcare.org) and the Director of Veterinary Programs and Research. She is an invited member of the Asian Elephant Specialist Group (IUCN), an author and co-editor of Biology, Medicine, and Surgery of Elephants (Blackwell 2006) and a co-author of Medical Management of the Elephant (Indira Publishing 1994). Dr. Mikota is a consulting veterinarian at the Elephant Sanctuary in Tennessee. She may be contacted at Elephant Care International, 166 Limo View Lane, Hohenwald, TN 38462, at smikota@elephantcare.org or at http://www.elephantcare.org.

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Chapter 7 Contemporary Zoo Elephant Management: Captive to a 19th Century Vision


Lisa F. Kane

Attorney and Co-Founder of the Coalition for Captive Elephant Well-Being The modern zoo industry has turned increasingly to science to inform policies concerning the exhibition of wild animals. Over the past 25 years, zoos have worked hard to transform themselves into green institutions offering open vistas of spacious, environmentally complex habitats containing natural family groups of wild mammals. This transformation was originally inspired by Swiss zoo director Heini Hedigers (1950) call to develop zoo environments that addressed behavioral, psychological and physiological needs of captive wild animals based upon the species natural history. Later, Eisenbergs seminal work (1981) contributed a useful model of mammalian life strategies that permitted systematic and coherent analysis of field data. His model organized thousands of disparate facts into meaningful, predictable patterns that described a species natural life cycle. Zoos have made strides both large and small in applying Hedigers perspective that while zoos cannot replicate the wild environment, species natural history plays an indispensable role in informing zoo design and species management strategies. It is not open to reasonable doubt that Eisenbergs model is scientifically sound and that Hedigers perspective contributes to the well-being of wild mammals in captivity. Their contributions have strongly influenced the thinking of zoo professionals, from architectural design (Coe 2003) to animal management theory and protocols (Kleiman, Allen, Thompson & Lumpkin 1996; Seidensticker & Doherty 1996; Forthman 1998; Seidensticker & Forthman 1998). Over the past 20 years, for example, great apes have benefited greatly (Maple, Bloomsmith & Martin, Chapter 10) from the change in their management and exhibition that resulted from a deeper understanding of the species provided by the application of Hedigers perspective as well as modern comparative primatology. Still, the enlightened decision by some to embrace Hedigers analytic approach and Eisenbergs model brings with it certain risks, for what may serve as a guide may also serve as a means by which to measure success. And theres the rub. While many North American zoos have revolutionized their exhibition and management of great apes and other species to account for their natural history and biology, the revolution has to date largely bypassed elephants. Close review of volumes of carefully detailed observations of free-ranging elephants social organization and size and the complexity of their living space is hardly required to observe that American zoosoverwhelmingly small, urban institutions holding one, two or three unrelated female elephants in small spaces with few natural featureslack the capacity to give elephants the range of environmental and social options that allow them to acquire the psychosocial, reproductive, physical or cognitive skills that define their species (Bradshaw, Chapter 4; Lee & Moss, Chapter 2; Poole & Granli, Chapter 1). This essay will explore the premises that: (1) although the Association of Zoos and Aquariums
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(AZA is the group representing the industry in North America) claims that its member zoos provide elephants in their care a high quality of life, the AZAs industry-wide Standards for Elephant Management and Care (2003) fail in key respects to account for existing scientific knowledge about elephants; (2) American zoos inability to innovate in response to scientific knowledge about elephant species behavioral biology is driven by most zoos urban location, economics and tradition; and (3) so long as zoos persist in ignoring elephants natural history and fail to collect empirical evidence on key questions about elephant welfare, elephants will suffer in zoos, and zoos will fail to educate the public or make a useful contribution towards conserving the extant species. Key AZA elephant management standards lack scientific foundation The common and popular presence of elephants in American zoos dates back to the 1800s, a time that predates our scientific knowledge of the species. Now we better understand their natural life cycle, their complex, yet stable social organization, and their use of large tracts of land over the course of their long lives. AZA zoos actively present themselves as institutions pursuing science and education aimed at improving the lives of elephants in their care and in the wild (Reed 2005). Regrettably, these claims find little objective support. Despite intense public debate and criticism of zoos on these points (Hutchins 2006), zoos have never gathered empirical data on fundamental questions related to space, social, occupational or other needs of elephants (Barber, Chapter 9; Maple et al., Chapter 10). Simultaneously, the zoo industry has largely ignored or dismissed scientific insights into elephants natural history carefully assembled over the past 35 years in detailed studies of elephant behavior, ecology, biology and social organization. Rigorous longitudinal research on elephants conducted by Douglas-Hamilton and DouglasHamilton (1975), Eisenberg (1981), Moss (1983), Lee (1986, 1987), Lee and Moss (1986, 1999, Chapter 2), Sukumar (1994, 2003), Payne (1998, 2003), Poole and Granli (Chapter 1) and others, provides ample foundation for standards envisioned to meet the challenge of preserving elephant social systems in rich physical environments. Based on the work of these field scientists, North American zoo professionals now know that in the wild, female elephants never live alone but remain in matriarchal family herds throughout their lives. Indeed, female elephants are renowned for close, lifelong relationships (Sukumar 2003; Lee & Moss, Chapter 2). The matriarchal herd, typically composed of three lineal generations, is the core social experience of all elephants. It is stable even in the face of severe competition for resources (Wittemyer, Douglas-Hamilton & Getz 2005). Although the North American zoo industry is undoubtedly conversant with this body of knowledge, AZA standards fail to acknowledge these key characteristics of elephant life. AZA standards fail to safeguard 1) the lifelong bond observed in the wild between mothers and their female offspring (Moss 1983; Sukumar 2003; Lee & Moss, Chapter 2); 2) the fidelity of relationships exhibited by female elephants (Lee & Moss, Chapter 2); and 3) the provision of a calf-rearing environment that consists of a stable, rich social context (Lee & Moss, Chapter 2). In contravention of scientific knowledge of elephant social organization, AZA standards allow male and female calves as young as three to be removed from their mothers, irrespective of cause (cf. Rees 2001; AZA 2003). Industry standards governing living space for elephants are another critical flash point in the ongoing debate between the zoo industry and animal protection community. Zoo exhibit and holding space for elephants illustrates its apparent inability to innovate in response to existing or new scientific knowledge and the industrys continued embrace of 19thcentury cultural attitudes
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and values. AZAs Elephant Management Standards require outdoor space of at least 1,800 sq. ft. (167.2 sq. m) for a single adult individual and an additional 900 sq. ft. (83.6 sq. m) for each additional animal (AZA 2003). Indoor space must provide 400 sq. ft. (37.2 sq. m) for a single animal, approximately 800 sq. ft. (74 sq. m) for two animals, and so on (AZA 2003). Bulls or cows with calves are granted a minimum of 600 sq. ft. (55.7 sq. m: AZA 2003). These standards are not influenced by climate. In other words, if an Asian elephant in upstate New York spends months on end inside his or her barn, the standards mandate no additional space. Moreover, industry reports state that 52 percent of AZAs members exhibiting elephants do not comply with even these low standards (AZA 2005). These space requirements bear no observable relationship to elephants known use of space in the wild, the animals size or the scale and length of their lives. The smallest African elephant home ranges reported by Sukumar are 14 to 52 sq. km (5.4 to 20 sq. m: 2003, p. 162). Sukumar reports surprisingly small home ranges among Asian family groups in the eastern dry zone of Sri Lanka at a mean range size of only 90 sq. km (34.7 sq. m: 2003, p. 165). AZA elephants frequent experience of arthritis, osteomyelitis and other chronic and fatal orthopedic disabilities is well-known (Mikota, Sargent & Ranglack 1994; Csuti, Sargent & Beckert 2001; Fowler 2001; Roocroft & Oosterhuis 2001). Foot disease is the leading cause of death among Asian elephants in captivity in North America. The grave consequences to elephants arising from their living conditions in zoos periodically erupt into the public consciousness. In 2006, two Asian elephants died in AZA zoos as a result of crippling arthritis, related bone degeneration and opportunistic infectionsToni at National Zoo and Gita at Los Angeles Zoo. A meta-review of health records of publicly owned zoos reveals that, since as recently as 1990, dozens of AZA elephants have died as the result of foot and joint disease and its complications (APHIS docket 2006-0044). AZA staunchly defends the size of its member zoos elephant exhibits. The chair of AZAs Elephant TAG committee, Oregon Zoo curator Michael Keele, has asserted, Theres zero science to support what kind of space is needed at this point in time (San Diego Union-Tribune, June 19, 2005). If Keeles statement is accurate, it necessarily follows that AZAs space standard, arguably one of its most important, is not based on science (as no science exists on the issue, according to Keele). The question is, then, what are AZAs space standards based on? One obvious answer is that the small, monotonous spaces allotted to elephants by AZAs standards acknowledge an industry-wide, immutable predicament: most zoos exhibiting elephants are situated in our urban centers, often on fewer than 40 acres, into which are crammed exhibit spaces for hundreds of animals. Most zoos have no ready means of expansion and are clearly unwilling to expand space for elephants by removing other exhibit spaces. The obvious consequence is that zoos cannot innovate in response to scientific knowledge about elephants. Given this common predicament, most zoos resist acknowledging relevant scientific data and reports, or the species natural history, biology and vital elements of their life history strategies (Lee & Moss, Chapter 2) that might suggest a responsibility to take action. Thus there exists the political necessity for zoos to avoid collecting empirical evidence that might help to answer the question of just how much and what sort of living space an elephant needs. Apparently fearing what empirical research might suggest on the issue of living space needs, zoos now argue that how much space an elephant might need is no longer a question requiring an answer, asserting instead that quality of space means more than the amount of space available (Maple et al., Chapter 10). This assertion is itself a theory for which the zoo industry has produced
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no supporting data. In any event, even when a zoo can afford to provide a challenging and complex quarter-acre or even the exquisitely rare full acre, an average elephant in the wild occupying an average home range can daily choose from hundreds of such seasonally variable quarter-acres or full acres scattered throughout its range, each of which will be more complex, containing other elephants, other animals, dozens of different plant species and topographical features and challenges, as compared to zoos essentially static exhibit spaces. The spaces allotted by AZAs space standards perpetuate an attitude prevalent in zoos since at least the early 19th century that zoos are for people (Siedensticker & Doherty 1996; Hanson 2002). Small spaces perpetuate zoos historic 19th century ideal of displaying wild animals for close inspection by their visitors. It appears that AZAs space requirements are based entirely on the handicap of most American zoos urban footprints and this simplistic philosophy. Sadly, there is little evidence of the industrys ability or willingness to innovate in the near future. Hugely expensive construction projects have been undertaken in recent years, and zoos nationwide have announced plans to spend hundreds of millions of dollars to build new, remarkably small elephant exhibits. Construction costs on just two projects tell the story: Los Angeles Zoo (where Gita, a 48-year-old Asian female, died in June 2006 from bone infections related to chronic arthritis and foot disease) will spend 40 million dollars to expand its elephant exhibit to about 3.5 acres while National Zoo (where Toni, a 39-year-old Asian female died in January 2006 from bone infections related to chronic arthritis and foot disease) announced its commitment to spend 60 million dollars for a new four-acre elephant exhibit. But even these exhibit dimensions overstate the future space available to elephants at these zoos. National Zoo and Los Angeles Zoo will sub-divide these multi-acre spaces into smaller corrals and yards, none of which will likely exceed one acre. These financial commitments demonstrate the confidence of these institutions, and approximately 40 other North American zoos that have announced plans for multi-million-dollar one- and two-acre expansion plans, that AZA space standards will not increase markedly within the next several decades, no matter what science exists or is discovered on the issue of elephants need for complex, non-static living spaces sufficient to accommodate a family group maintained together and engaged in a reasonable facsimile of their life history strategies in the wild. How are zoo elephants faring compared to free-ranging elephants? Veterinary medicine and science agree that captive wild mammal welfare is best evaluated against a background of the fitness and behavior of wild free-ranging populations (Dawkins 1980). Over the past 30 years, Moss has collected baseline data painting a detailed picture of the normative behavior and health of the elephants in Kenyas Amboseli National Park. She and her team recorded 35,000 observations of a total sample size of 2,200 individuals (Moss unpublished longterm records). When benchmarks of life expectancy, fertility and social and reproductive success are examined, it appears that elephants held by the American zoo industry are faring poorly by comparison to their free-ranging counterparts in southern Kenya, despite the awful human-made and natural problems faced by the latter. African elephant life expectancy Lee and Moss report (Chapter 2) that female members of the Amboseli population have an average life expectancy of 54 years, while males enjoy a life expectancy of 42 years. In contrast, Willis and Wiese (2005) report an average life expectancy of only 33 years for African elephants in
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AZA zoos. It is noteworthy that elephants in North American zoos are protected from drought and human predation, the two main causes of premature death in the free-ranging elephants Lee and Moss studied. Elephants in zoos are also, unlike their free-ranging counterparts, the beneficiaries of cutting-edge veterinary care. Still, they are dying on average 20 years younger. These data suggest that our zoos environmental conditions and management approaches fail to provide even minimal welfare to the captive elephant population. Elephants social skills and health Reviewing some key discrepant details between elephants behavior and health in the wild and in North American zoos paints a similarly dark picture. Moss reports no infanticide or calf rejection by mothers, two cases of infertility out of 558 females over the age of 10, no stereotypic behavior and no foot or weight problems in the Amboseli elephants (Moss unpublished long-term records). In contrast, AZA zoos report that 30 percent of their females of calf-bearing age are infertile (Freeman 2004). Zoos commonly report captive elephant foot health and weight problems; indeed, these heath conditions have been the special subject of scrutiny in professional zoological treatises (see e.g., Csuti, Sargent & Bechert 2001; Clubb & Mason 2002). AZA zoos also report maladaptive and stereotypic behavior by their elephants. In a special issue of Zoo Biology, Brown (2000) wrote that infertility, maternal rejection, infanticide and high infant mortality rates predict the extinction of all elephant species in North American zoos within only a few decades. In keeping with Browns prediction, Keele reported that the population of elephants in North American zoos will continue to decline unless captive reproduction rates and importations of wild-caught animals increase (Keele unpublished data 2005). What might account for poor rates of reproductive success and longevity of captive-born animals? One explanation is that human-engineered elephant breeding programs as conducted in zoo environments are physically and socially stressful for elephants. It is important to remember that many American zoo environments have remained unchanged in material respect for well over a century. A majority of elephants in North American zoos spend a majority of their time indoors on concrete, whether their outdoor corral is one-quarter acre or five acres in size (Csuti et al. 2001). Elephants held in cold climates can spend up to five months indoors. Elephants held in climates for which they are adapted nevertheless often spend 17 hours a day indoors on cement year round due to zoo staff limitations and managers reluctance to allow animals unsupervised outdoors access overnight (Kane, Forthman & Hancocks, Appendix I). Second, socially skillful, reproductively successful, stable, multi-generational cow-calf herds are virtually non-existent in North American zoos. Nor can the advent of such herds be expected since nothing in AZAs Elephant Management Standards protects nor promotes the lifelong bonds that underlie such herds in the wild. Finally, zoo environments appear to be lethally inhospitable to elephant calves. In September 2003, Keele reported at AZAs annual conference that a total of 40 calves were born as the result of AZAs SSP captive African elephant program from its inception through June 2003 (Keele unpublished data). He went on to state that only 13 of these animals were still alive (Keele unpublished data 2003). Keele reported in September 2005 at AZAs annual conference that one African calf was born in the prior 12 months; the infant did not survive. The contrast between the reproductive successes of elephants held in Americas best zoos and the experience of their counterparts in the wild, when left largely undisturbed by rampant human
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predation, is stark. Elephant populations flourish in the wild despite predation, drought and even some poaching. African elephants residing in large national parks and preserves, like the Amboseli population, are able to utilize living space year round that supports their life strategies and social organization on hospitable terrain. The Amboseli population, for example, has doubled in size over the past 30 years to its present census of 1,400 individuals (Moss unpublished long-term records).In South Africa, the elephants reproductive rate is reported at an impressive five percent per annum (van Aarde & Jackson 2007). American zoo culture: insular and tradition bound It is hard to avoid the conclusion that captivity as envisioned and practiced by modern American zoos does not provide elephants with what they need to flourish. In fact, the data on fertility and population growth of elephants in our zoos suggest that a majority of contemporary zoos fail to provide the environmental and management approaches conducive to minimal elephant welfare. So what might explain Americas zoos manifest difficulties? One clue might be found in the professional insularity of North American elephant management programs. For decades, these programs have largely relied on in-house salaried veterinary staff and the circus industry for guidance rather than seeking independent scientific collaboration with academic institutions. Salaried veterinarians and paid consultants Zoos typically enlist the assistance of their veterinary staff and a few trusted private consultants to make up for the impoverished social and occupational options offered by small exhibit spaces. Seidensticker and Doherty (1996) identified this zoo management model a decade ago as the medical management model, one that emphasizes direct human technological intervention to help animals in captivity remain healthy. This approach focuses on fixing animals so that they can adjust to conditions rather than adjusting conditions of confinement to meet the needs of the animal. The medical management model is pervasive in North American zoos and for good reason: the model permits zoos to sidestep questions critical to industry assumptions regarding space and management approaches. It allows North American zoos to emphasize direct human technological intervention and uncritically promotes artificial captive elephant breeding. An excerpt from the St. Louis Zoos current elephant management manual exemplifies the model: When the first signs of labor appear, the elephant handlers will tether the elephant on 3 or 4 leg restraints (chain or rope). It is recommended that inexperienced or nervous elephants be tethered so the newborn can be pulled if the mother becomes excited. Inexperienced elephants have rejected or even killed newborns.The newborn calf will be immediately removed from the mother.The female is allowed to calm down as she watches her infant being attended to.This period of separation gives the female time to recover from the shock of birth, gives the staff time to clean and inspect the baby, the veterinarian time to perform the neonatal exam and the baby time to become steady on its feetThe rest of the herd will be in adjacent stalls to avoid interfering with the elephant care staff but still observe the birth and newborn calf.It is important for all females to witness the birth and after-care as this is an invaluable learning experience. They may also need to be tethered if they become agitated.
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Ironically, the broad application of the medical model is demonstrably ineffective when it comes to elephants. Although the industrys efforts to breed elephants come at a huge financial cost, these mechanistic, human-dominated efforts have yielded birth rates too low to maintain North Americas small captive population. Zoos report a dismal neonatal death rate of approximately 30 percent (Brown 2000; Willis & Wiese 2004), as compared to seven percent reported in free-ranging populations in Amboseli (Moss 1983), where calves are born to mothers supported by experienced, older family members and eager young allomothers (Lee & Moss, Chapter 2). Still, the zoo industry persists in this management approach. Staff professionals and consultants enjoy little incentive to raise questions or articulate objections. The North American zoo industry made its position clear: diverse points of view are not tolerated within an industry that repeatedly warns its elephant holding institutions that they must speak with one voice (AZA 2005). Circus industry values and traditions A serious impediment to a genuine infusion of science into zoo operations may be its incompatibility with the circus culture embraced by leading managers of zoo elephant programs. United in the view that elephants are integral to their respective financial success, zoos and circuses have engaged in mutually beneficial practices, such as exchanging and trading elephants, since the 19th century (Hoage & Deiss 1996; Hanson 2002). In addition to the exchange of animals, there was and remains a significant overlap between circus people, animal dealers, and zoo employees (Hanson 2002, p. 83). This overlap has resulted, in part, with a continued infusion of circus industry practices, values and vision into zoos. For example, both industries are dedicated to providing the American public an intimate physical encounter with elephants. As a result of this shared vision, zoos and circuses are committed to managing their elephants intensively and to displaying them in small spaceswhether a circus ring or outdoor zoo exhibitso that they may be easily and reliably viewed by the public, irrespective of virtually all physical or psychological cost to the elephants. Both industries are anxious to breed elephants because elephant babies are huge magnets for public interest and increased gate receipts (AZA 2001). The overlap of zoo and circus staff at the highest levels of both industries continues to this day. Key players in both the North American Zoo and circus industries sit together on the board of the International Elephant Foundation (IEF), AZAs official partner in distributing money to in situ conservation efforts. Key individuals dominating AZAs Elephant TAG steering committee lack advanced academic credentials, whether in animal science, animal behavior or conservation biology. A brief survey in 2005 disclosed that advisory groups serving the Elephant TAG steering committee were largely composed of zoo industry employees or paid consultants. For example, the advisory group on training had three members, all from zoos utilizing free contact, a management system employed by all circuses and dependent upon chaining, the ankus and human domination (Kane, Forthman & Hancocks, Appendix I; Whittaker & Laule, Chapter 13). Five members of the AZA advisory group on research were employed either by zoos or circuses; only the sixth member came from a university. The advisory group on reproduction had six members with, again, only one member from an arguably independent university background. However, this member was a leading exponent of artificial insemination of elephants and operated a reproduction consulting business heavily patronized by American circuses and zoos. Perhaps the best evidence of the intense and mutually beneficial relationship between zoos and circuses came in testimony from a long-time leader on the Elephant TAG steering committee
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in opposition to a House of Representatives Bill to ban performing elephants and elephant rides in 1999: A partnership exists as zoos work with those who travel with elephants, the circuses and private individualsCircuses developed many of the training skills we used to condition our elephants for the artificial insemination procedure. In fact most zoos directly employ these skills in the management of their elephants today The professional alliance between zoos and the circus industry is uniquely American. Professional European and UK zoos have no similar symbiotic relationship with the European circus industry (Fred Kurt, pers comm. Feb. 12, 2006), and neither do Australian zoos, although they never chose to criticize the practice of maintaining wild animals in circuses (David Hancocks, pers. comm. Feb. 14, 2007). So long as this American anomaly continues, there is little reason for optimism that visible strides will be made in moving the zoo industrys management and treatment of elephants onto a more scientific footing. Do zoos educate the public about elephants? Zoos defend their traditional mode of elephant exhibition in part by asserting that seeing elephants close up provides a unique and valuable educational experience for millions of guests. However, even a cursory review of this claim suggests no measurable education is occurring. Zoos have long trumpeted their mission to educate the public as evidence of their serious cultural purpose. AZA zoos in particular disseminate a carefully crafted public message claiming conservation education as a core mission. However, nothing in the presentation of elephants in most AZA zoos communicates their powerful physical vigor, the lifelong relationships binding related females together in family units, or their amazing cognitive and problem-solving abilities. Only their most superficial characteristicstheir size, color and shapeare put on display. Empirical evidence measuring the knowledge imparted by zoos to their guests bears this out. In 2001, AZA set out to investigate and measure the overall impact of visits to AZA zoos and aquariums on visitors conservation-related knowledge, attitudes, affect and behavior (Dierking, Burtnyk, Buchner & Falk 2001-2002, p. i). The report, Visitor Learning in Zoos and Aquariums, disclosed that AZA zoos have produced almost no evidence of measurable educational impact on the public. Although many industry studies cited the potential for zoos to positively influence their visitors conservation knowledge, affect, attitude and behavior, these claims were not substantiated or validated by actual research (Dierking et al. 2001-2002, p.vi). The authors of the report characterized zoo visitors conservation knowledge as superficial (Dierking et al. 2001-2002, p.3). To date, AZA has presented no empirical data contradicting these conclusions (Williamson, Chapter 18). Interestingly, it appears that the public is not looking for a serious educational experience when visiting zoos. Anne Baker, 2003-2004 president of AZA, reported in the AZA newsletter, Communique, that A recent survey of our visitors here at The Rosamond Gifford Zoo showed that the top two reasons people visit our zoo are to spend quality time with their family and to have fun (2003, p. 3). In fact, according to industry studies summarized by Croke (1997), the most common zoo visitor is a married woman under thirty who is accompanied by a child or children [W]e know that she will breeze through the exhibits; she wont read many informational signs. And she will buy snacks and drinks. Young families represent the largest segment of visitors to American zoos. Fully 25 percent of all visitors are children six or younger. Sixty percent of adults are females and 75 percent of all adult visitors are married. These zoo visitors tend to spend one to
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three minutes per exhibit (Croke 1997, p. 97). What might the typical zoo visitora young woman with one or two preschool-age children in towlearn from their brief pause before a typical elephant exhibit in pursuit of family quality time and fun? Whether visitors see zoo elephants indoors or outdoors, most elephant exhibits teach the public very little, if anything, about elephants biology, social system, complex communicative abilities or their unequalled physical strength and endurance. AZA zoos elephant exhibits commonly hold two or possibly three unrelated sedentary female adults standing in small, unyielding, monotonous spaces with little to engage them. Elephants in zoos rarely, if ever, have access to grass or trees, although fresh browse may be provided (Kinzley, Chapter 12). Indoor elephant exhibits, where most zoo elephants spend the majority of their time, are smaller, even more unnatural and lacking in anything of value to the elephantsbeing typically composed entirely of reinforced concrete and steel forms. The poverty of elephant exhibits is ubiquitous, whether the animals are Asian or African in origin. No AZA Asian elephant exhibits provide their elephants anything resembling the complex spatial, visual or tactile qualities of the wet, lush tropical and semi-tropical forests of their home range countries. The same is true for exhibit spaces for African elephants in AZA zoos compared to their native savanna or forest ranges. In short, most North American exhibits bear no visual, ecological or other resemblance to real Asian or African habitat or the ways in which Asian and African elephants lead their lives in the wild (Hancocks 2001, p.122). In response to growing public criticism of its elephant management practices and the dismal results of the Dierking et al. (2001-2002) study, AZA recently hired the Harris/Roper organization to poll the American public. AZAs poll reports that 95 percent of American adults reported that seeing elephants in a zoo has given them a greater appreciation of elephants. AZA prominently displayed this favorable poll number on its website, press releases and elsewhere, apparently attempting to position its poll as actual research (Dierking et al. 2001). One need not be a social scientist to predict that most people are likely to assert that they have a greater appreciation of elephants after visiting a zoo. The real issue is whether their newfound appreciation consists of a deeper understanding and awareness of the life history of elephants, or increased respect for their intrinsic value and an increased desire to promote their well-being, as demonstrated by changes in the zoo visitors behavior. Regrettably, the poll fails to correlate visitors appreciation with visitors conservation knowledge, affect, attitude and behavior (Dierking et al. 2001-2002). AZAs recent study, Why Zoos & Aquariums Matter: Assessing the Impact of a Visit to a Zoo or Aquarium, reports that visitors to zoos brought higher-than-expected knowledge about basic ecological concepts. A small percentage group of visitors (approximately 10 percent) did show significant changes in their conservation-related knowledge. However, because of the higher than expected entering knowledge of most visitors, there were no statistically significant changes in overall knowledge (Falk, Reinhard, Vernon, Bronnenkant et al. 2007, p. 10). At its most optimistic, the report states that visits to zoos reinforced and supported pre-existing attitudes and values of their guests. It appears, therefore, that the zoo industrys cherished claim that its member zoos are important centers of conservation education remains an unproven hypothesis. Zoos parsimonious commitment to in situ elephant conservation Sadly, there is little of comfort when it comes to the North American zoo industrys contribution to in situ elephant conservation. The lack of robust funding by zoos for conservation efforts that
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could directly benefit free-ranging elephants speaks in the plainest possible terms to zoos inability to inspire their visitors to give money for elephant conservation. The IEF, AZA zoos official partner in identifying and funding elephant conservation projects worldwide, awarded grants for elephant conservation amounting to $110,000 in 2005-06 out of a total of 1.1 million dollars over the past decade for such purposes (AZA 2007). Given the annual expense of maintaining elephantsput at $57,900 per year per animal or a collective expenditure AZA-wide of $3,995,051 on its elephants per annumthese IEF/AZA awards are parsimonious in the extreme. And compared to the more than 300 million dollars in construction budgets recently announced by AZA zoos, industry-wide grants totaling 1.1 million dollars awarded over the past approximately 10 years for in situ conservation would be laughable if the plight of elephants in the wild were not so desperate. In any event, such paltry sums undermine the strength of AZAs claim of wildlife conservation as a core mission. Finally, independent elephant experts recognize that captive breeding and management by American zoos and circuses are not instruments of conservation of the species: Believing there to be no direct benefit for in situ conservation of African elephants, the African Elephant Specialist Group of the IUCN Species Survival Commission does not endorse the removal of African elephants from the wild for any captive use (IUCN/SSC December 2003). Conclusion AZAs leadership appears intent on continuing down a path of elephant management strategies and exhibition philosophies materially unchanged since the 19th century. As presently conceived, this vision locks elephants into small spaces bereft of biophysical options and under management schemes that deny them psychosocial support, stability or autonomy. Until the North American zoo industry admits the light of science and the vigor of independent expertise into its tradition-bound, insular world of elephant management, the elephants in its care will continue to be little more than forlorn, chained captives, so-called ambassadors from the wild, marking time before the publics eyes until death releases them. Acknowledgments I wish to express my deep gratitude to Gary Fink for his loyalty, inspiration and generous support over many years. I also wish to thank Robert Atkinson, Carol Buckley, Debra Forthman, David Hancocks, Lisa Sherman, Peter Stroud and Paul Waldau for their kind friendship and wise counsel. Finally, I wish to thank Winkie, Penny, Joy and Maggie for immeasurably enriching my life. This chapter is dedicated to them and, most importantly, to Larry, Kristin and Elliott.

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AZA. 2003. Standards for elephant management and care. Silver Spring, MD: AZA. AZA. January 2007. Support for elephant conservation tops $1.1 million. Retrieved on Sept. 17, 2007 from http://www.aza.org/Newsroom/PR_SupportElephCons/. AZA Regents. 2001. AZA school for zoo and aquarium personnel: principles of elephant management. Silver Spring, MD: AZA. AZA. 2005. Survey results: AZA directors elephant workshop summary. Unpublished pamphlet. Baker A. 2003. From the president. Communique, December, 3(54). Silver Spring, MD: AZA. Brown JL. 2000. Introduction to the special issue on elephant biology. Zoo Biol 19:297-298. Clubb R, Mason G. 2002. A review of the welfare of zoo elephants in Europe. Horsham, UK: RSPCA. Coe J. 2003. Steering the ark toward Eden: design for animal well-being. JAVMA 223(7) 977-980. Croke V. 1997.The modern ark: the story of zoos past, present and future. New York, NY: Avon Books. Csuti B, Sargent EL, Bechert US, eds. 2001. The elephants foot. Ames, IA: Iowa State University Press. Dawkins MS. 1980. Animal suffering: the science of animal welfare. London, UK: Chapman and Hall. Dierking LD, Burtnyk K, Buchner KS, Falk J. 2001-2002. Visitor learning in zoos and aquariums: executive summary and a literature review. Silver Spring, MD: AZA. Douglas-Hamilton I, Douglas-Hamilton O. 1975. Among the elephants. New York, NY: The Viking Press. Eisenberg JF. 1981. The mammalian radiations: an analysis of trends in evolution, adaptation, and behavior. Chicago, IL: University of Chicago Press. Falk JH, Reinhard EM, Vernon CL, Bronnenkant K, Heimlich JE, Deans N. 2007. Why zoos and aquariums matter: assessing the impact of a visit to a zoo or aquarium. Silver Spring, MD: AZA. Forthman DL. 1998. Toward optimal care for confined ungulates. In: Shepherdson DJ, Mellen JD, Hutchins M, eds. Second nature: environmental enrichment for captive animals. Washington, DC: Smithsonian Institution Press. p. 236-261. Fowler ME. 2001. An overview of foot condition in Asian and African elephants. In: Csuti B, Sargent EL, Bechert US, eds. The elephants foot. Ames, IA: Iowa State University Press. p. 3-7. Freeman EW, Weiss E, Brown JL. 2004. Examination of the interrelationships of behavior, dominance status and ovarian activity in captive Asian and African elephants. Zoo Biol 23:431-48. Hancocks D. 2001. A different nature: the paradoxical world of zoos and their uncertain future. Los Angeles, CA: University of California Press. Hanson E. 2002. Animal attractions: nature on display in American zoos. Princeton, NJ: Princeton University Press. Hediger H. 1950. Wild animals in captivity. London, UK: Butterworth. Hoage RJ, Deiss WA. 1996. New worlds, new animals: from menagerie to zoological park in the nineteenth century. Baltimore, MD: Johns Hopkins University Press. Hutchins M. 2006. Variation in nature: its implications for zoo elephant management. Zoo Biol 25:161171. IUCN/SSC African Elephant Specialist Group. December 2003. Statement from the African elephant specialist group of the IUCN species survival commission on the removal of African elephant for captive use. Retrieved on July 15, 2007 from http://www.iucn.org/themes/ssc/sgs/afedsg/tools/pdfs/ pos_capvuse_en.pdf. Kleiman DG, Allen ME, Thompson KV, Lumpkin S, eds. 1996. Wild mammals in captivity: principles and techniques. Chicago, IL: University of Chicago Press. Lee PC. 1986. Early social development among African elephant calves. Nat Geo Res 2:388-401. Lee PC. 1987. Allomothering among African elephants. Anim Behav 35:278-91. Lee PC, Moss CJ. 1986. Early maternal investment in male and female African elephants calves. Behav Ecol & Sociobiol 18:353-361.

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Lee PC, Moss CJ. 1999. The social context for learning and behavioural development among wild African elephants. In: Box HO, Gibson KR, eds. Mammalian social learning. Cambridge, UK: Cambridge University Press. p. 102-125. Mikota SK, Sargent EL, Ranglack GS. 1994. Medical management of the elephant. West Bloomfield, MI: Indira Publishing House. Moss CJ. 1983. Elephant memories. New York, NY: William Morrow. Payne K. 1998. Silent thunder. New York, NY: Penguin Books. Payne K. 2003. Sources of social complexity in the three elephant species. In: De Waal FB, Tyack PL, eds. Animal social complexity: intelligence, culture, and individualized societies. Cambridge, MA: Harvard University Press. p. 57-85. Poole T. 1998. Meeting a mammals psychological needs: basic principles. In: Shepherdson DJ, Mellen JD, Hutchins M, eds. Second nature: environmental enrichment for captive animals. Washington, DC: Smithsonian Institution Press. p. 83-94. Reed MC. 2005. From the president. Communique, March. American Zoo and Aquarium Association, Silver Spring, MD. Rees P. 2001. Captive breeding of Asian elephants (Elephas maximus): the importance of producing socially competent animals. In: Hosetti BB, Venkateshwarlu M, eds. Trends in wildlife biodiversity, conservation and management. Delhi, India: Deya Publishing House. p. 76-91. Roocroft A, Oosterhuis J. 2001. Foot care for captive elephants. In: Csuti B, Sargent EL, Bechert US, eds. 2001. The elephants foot. Ames, IA: Iowa State University Press. p. 21-52. Seidensticker J, Doherty JG. 1996. Integrating animal behavior and exhibit design. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S, eds. Wild mammals in captivity: principles and techniques. Chicago, IL: University of Chicago Press. p. 180-190. Seidensticker J, Forthman DL. 1998. Evolution, ecology, and enrichment: basic considerations for wild animals in zoos. In: Shepherdson DJ, Mellen JD, Hutchins M, eds. Second nature: environmental enrichment for captive animals. Washington, DC: Smithsonian Institution Press. p.15-29. Steele J. 2005. Where do elephants belong? Zoo industry, animal rights groups differ over what constitutes humane treatment of captive pachyderms, San Diego Union-Tribune, June 19. Sukumar R. 1994. Elephant days and nights. Delhi, India: Oxford University Press. Sukumar R. 2003. The living elephants. New York, NY: Oxford University Press. van Aarde RJ, Jackson TP. 2006. Megaparks for metapopulations: addressing the causes of locally high elephant numbers in southern Africa. Biol Conserv 134:289-297. Wiese RJ, Willis K. 2005. Calculation of longevity and life expectancy in captive elephants. Zoo Biol 23:365373. Wittemyer G, Douglas-Hamilton I, Getz WM. 2005. The socioecology of elephants: analysis of the processes creating multi-tiered social structures. Anim Behav 69:1357-1371.

Lisa Kane, JD, a practicing attorney, began her legal career as counsel to the Wisconsin Department of Agriculture, specializing in animal health and meat inspection issues. She has written, traveled and spoken on elephant issues since 2002. She presently serves on a panel of elephant welfare experts advising University of Bristol researchers charged with investigating zoo elephant welfare in the United Kingdom and Ireland. She may be contacted at 2055 Floral Dr., Boulder, CO 80304 or at lkane11550@yahoo.com.

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Peter C. Stroud Zoological Consultant

Elephants are wild creatures and, not having been selectively bred by man for generations, they cannot be expected to alter their habits in every particular at a moments notice to suit mans requirements, so that, if an officer finds that he cannot, for any reason, accommodate himself to the habits of the elephant, he should dispense with this form of transport. There does not appear to be any other alternative. A.J.W. Milroy At the beginning of the 21st century, elephants are still treated by many Western zoos as if they are domesticated animals, modified in behavior by human agency to suit human purposes. In taking such an approach, zoos actually depart from more progressive trends in wild animal husbandry. Elephants represent an anomaly. Zoos observe and explain elephant behavior within the narrow boundaries of their experience. The ability of elephants to submit to human control and to live in artificial conditions is used, a priori, to justify such conditions. This presents those arguing for a broader approach to defining elephant welfare with a dilemma. It is often argued that the artificial conditions of zoos are actually injurious to elephant health and well-being. Statistics can be performed to show that elephants in zoos live relatively short lives plagued by mental and physical ill health (Clubb & Mason 2002). Equally, zoos counter these arguments with claims of improving trends in lifespan and reproduction (Lees 2004; Weise & Willis 2004) and an ongoing emphasis on behavioral enrichment to improve mental health (Standley & Embury 2004; Stevenson & Walter 2006). Such a clash of arguments can further obscure rather than clarify sensible conclusions about the conditions elephants really need if they are to be maintained in captivity. Further complicating the picture, the goal of zoos to manage self-sustaining populations of elephants raises moral and ethical questions about the welfare of individual elephants versus the genetic and demographic health of populations. The elephant anomaly The husbandry of wild animals in Western zoos is a culturally embedded activity. The human view of animals in the zoo is tied to time and place and prevailing culture. From the mid-20th century, Dr. Heini Hediger became the zoo worlds clearest exponent of principles for how the care of wild animals in captivity should be approached. The standard by which a zoo animal is judged should be the life it leads in the wild under so-called free conditions of nature (Hediger 1969, p. 1, emphasis added). He went on to say, In the zoowe must take care to counteract all domestication phenomena; the wild animals loaned to us from nature must be
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kept in the most pure and original condition (Hediger 1969, p. 63, emphasis added). In the 1980s, these ideas were echoed by the American Zoo and Aquarium Association (AZA) in its Zoological Park and Aquarium Fundamentals (Sausman, Ed. 1982). In a chapter on the husbandry of mammals, Lawrence Curtis wrote (1982, p. 246), The zoo biologist must develop a solid understanding of individual species biology and ethology in the wild, supplemented by data gleaned from captive experience. Following such principles, in the absence of hard scientific facts about captive needs, zoos should be expected to draw reasonable inferences from what is known about wild animals, and then to test these inferences against the results of research. This is how progressive zoos approach the husbandry of the species in their care. Initial estimations of how animals intrinsic needs can be met are adjusted both on the basis of results (experience) and, crucially, on the basis of emerging knowledge of the biology of the species in the wild. Why then are elephants treated differently? To illustrate how elephants have been managed in Western zoos we need only look to the size of the social groupings in which they are maintained. Elephants are highly social mammals that spend their entire lives enmeshed in a complex web of relationships with dozens of other individuals (Sukumar 2003). These relationships are not confined to immediate family members. Considering the subset of European and North American zoos that have registered their collections with the International Species Information System (ISIS), freely available data indicate that 93 institutions keep cow Asian elephants (Elephas maximus). Of these, some 65 institutions keep fewer than four cows and a startling 51 institutions maintain fewer than three cows (ISIS 2006). The question must be asked, why does this patently unnatural situation pertain? In answering this question, qualifications are used frequently in some of the arguments offered from the contemporary zoo world. One line of reasoning holds that we can define elephant needs in captivity according to choices that the elephants themselves make and the individual behavioral traits that they exhibit towards other elephants, their human caregivers and their environment. This argument is hollow because elephants in captivity have all been shaped by their captive experiences from infancy and cannot indicate their natural preferences to us. Another line of argument involves a revisionist approach to the relevance of biology in determining the needs of wild animals in captivity. Hutchins (2006, p. 161-171) has argued that, making direct comparisons between wild and zoo animals may be a slippery slope, at least from a scientific perspective. He goes on to argue that variation in nature means that there is, no one nature for a particular species, no simplified categorization of the natural world that we can use as a model for either developing or evaluating the quality of zoo animal management programs. This, curiously, seems to argue that key characteristics cannot be ascribed to individual species. The inherent flexibility of species suggests to Hutchins that welfare for elephants can be defined only within a range of conditions that the species is able to tolerate. There are many problems with Hutchins approach, perhaps best exemplified by the way he describes optimum group size in elephants. Here he fails to recognize that while the size of a group overall is flexible, such groups are always a reflection of a web of complex social relationships that exist through extended periods of time and space (Sukumar 2003). The real reasons for the anomalous treatment of elephants are to be found in aspects of their biology. Field science now makes clear that elephants are unique amongst non-primate land mammals in the extent and scope of their learned behavior, their intelligence, the strength of their social bonds, the complexity of their communications, their tolerance of one another and their relative passivity as herbivores (Sukumar 2003). These very characteristics, however, leave elephants open to intense manipulation by human beings.
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Tradition and welfare Elephants have lent themselves to use by humans as beasts of burden, sacred beings, war machines, pets and status symbols. The Western zoo tradition itself appears to be narrowly derivative of the far older elephant-keeping cultures that in Asia date back at least 4,000 years. But this long tradition of elephant use has at its heart an economic equation. Elephants serve human ends and human needs. It is likely that humans would have farmed elephants were it not for the fact that because they take so long to mature and were so readily captured from wild stocks it was never economical to do so (Diamond 1998, p. 169). The most ancient traditional view is essentially utilitarian, even where it is embedded in notions of the sacred. The welfare of the elephant is framed by a need to support its continued use by humans. While we might expect that the long history of elephants-in-human-use has honed the treatment of elephants to ensure their health and survival, if this has been the case, it has been for human purposes. Where these purposes are no longer valid it should not surprise us that those standards of elephant care and welfare have eroded. There is clear evidence of this in Southeast Asia in the present day, where many elephants are underemployed or overworked (Lair 1997). It is arguable that tradition, even in Asia, has neither fulfilled intrinsic elephant welfare needs, nor has it ever set out to do so in any encompassing sense. It is equally arguable that in the past, during periods of stability in so-called traditional societies, elephant care, if considered holistically, was probably better than it is today in countries where elephants are still a part of economic life. Borrowing from and adapting ancient traditions, zoos from their beginnings in the 19th century have kept and displayed elephants of both Asian and African species, essentially as if they were work animals. Methods of containment and control have involved not only the physical apparatus of the zoo exhibit, but specific training of elephant and keeper to enable command and control of the animal both within and outside the confines of the elephant facilities. This training has been based on practices taken directly from Asian traditions; indeed, elephant trainers from Asia have in some instances found employment training elephants in zoos. It is quickly apparent that this zoo tradition brings with it fundamental issues: if the methods employed to manage elephants are based upon the requirement for the animal to perform work, how much work is there to occupy elephants in zoos and what does this mean for the construction of a definition of elephant welfare? What is the nature of this work and can it provide a zoo elephant with the sort of mental and physical health and development that substitute for a traditional life of work in Asia or for life in the wild? Answering these questions exposes the paradox at the heart of the traditional approach to the management of zoo elephants. Because elephant cultures have relied upon the capture of wild elephants to maintain captive stocks, there has been little requirement to foster breeding and maternal care of offspring. Asian elephants in their range countries today do not experience a social life in any way analogous to that experienced by their wild counterparts (Lair 1997). The same is true of elephants in Western zoos. Furthermore, it is likely that in practically all zoos where they are kept, elephants are more constrained and less occupied than traditionally managed captive elephants in Asia. Even considered by the traditional standards implicit in the urban zoo management of elephants, zoo elephants are underemployed. A further question we must ask, therefore, is, If for some thousands of years elephants have survived in captivity without access to natural social conditions and essentially under the control of human caregivers, should we conclude that an acceptable definition of what constitutes elephant welfare must recognize the inherent adaptability of elephants? More particularly, we should ask, Is it appropriate for zoos to construct a definition of zoo elephant welfare on this basis?
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As we have noted, removal of an elephant from its mother at a young age means that many of its responses will be conditioned by the treatment it receives in the zoo. These responses, and indeed mere survival and physical health, cannot alone reflect elephant needs. We may reasonably contend, therefore, that the answer to both questions is No. Such a construction essentially accepts prevailing conditions of limited space in urban environments and interventionist regimes of care to prompt elephants to gain some measure of physical and mental exercise. It fails to account in any systematic way for elephant biology and ignores an ethical consideration of how the individual elephant understands a world far removed from that in which elephants have evolved to function. It denies in very large measure any independent agency to the elephant to such an extent that even the social functioning of the individual, in any naturalistic way, is prevented, corrupted or both. Even from a narrow utilitarian standpoint we can conclude that as no humans depend on zoo elephants for their well-being, there can be no justification for approaching zoo elephants, tacitly or explicitly, as work animals. The history of elephants in zoos shows that tradition is an unreliable guide to captive elephant welfare. Whatever current trends may be, even real improvements in zoo elephant health, reproduction and longevity leave us with an anomalous situation. We may ask, What other social mammals have their natural social order so disregarded? Guidelines that recommend minimum group sizes of three or four females (AZA 2003; Standley & Embury 2004) do not begin to address the issue of natural social groupings for elephants in captivity. Neither does a genetic and demographic model that depends on artificial reproduction where elephants do not breed but are trained to be bred. Both of these approaches are designed entirely to serve the institutional philosophy and physical constraints imposed by most zoos. Here again it is the elephant that must adapt. At play is the old paradigm of the elephant in human use. Measurement of elephant welfare must include more than lifespan and reproduction. It must include an assessment of elephant-to-elephant social well-being in the context of family life over generations. What is really required is that independence, motivation and challenge are restored to captive elephants. Occupational therapy There is a growing emphasis in zoos on increasing the time that elephants and other animals spend in occupation in order to improve their mental and physical health. In the case of elephants specifically, this enrichment often involves giving them small problems to solve or simple physical exercises to perform in order to obtain rewards of food. We may contemplate the extent to which enrichment activities constitute just another form of work. Such activities do seem to reduce the observed levels of stereotypic behavior, at least in the time during which the activities are offered (Clubb & Mason 2002, p. 229-230). However the relationship between stereotypy and individual welfare is complex (Clubb & Mason 2002, p. 223), and those enrichment activities that are really beneficial to captive elephants are yet to be distinguished from those that may merely obscure the problems that elephants face in highly confined zoo environments. The incidence of stereotypic (aberrant) behaviors in animals is generally higher in close confinement than it is in more extensive and complex situations (Broom 1991, p. 4173). Clubb & Mason (2002, p. 227230) list as possible causative factors of stereotypic behavior in captive elephants, restriction of movement, social factors, complexity of the physical environment and foraging motivation. Of these factors, foraging motivation may be particularly significant given that elephants naturally spend 40 to 70 percent of each 24-hour period in feeding (Sukumar 2003, p. 198). Research into the causes of elephant stereotypies would help define the causes of aberrant elephant behavior and
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ill health in zoos, as well as delineate the practices that really benefit captive elephants from those that merely appear to do so. In the end, the impartial observer is left with a choice: accept that traditional systems of elephant management, established for utilitarian purposes, are adequate for meeting the welfare needs of zoo elephantseither as they are or with relatively minor adjustmentsor accept that field work now enables a more insightful approach based on the biology of wild elephants. If the latter choice is made, then the central questions should be, What is the form and function of this animal? What environmental forces have shaped it and to what ends? How does the elephant construct an understanding of its world? The goal of zoos should be to make captive elephants more like wild elephants. They should seek to establish conditions in which elephants can be elephants, conditions that are analogous to the wild, allowing the expression of as full a range of behaviors and activities as are required to support the natural development of each individual as a socially functioning entity independent of direct human manipulation and control. This goal needs careful discussion and refinement, with, above all, the critical guidance of field scientists who are expert in the biology of elephants. We might propose an outline of the fundamental characteristics of the species, the things about elephants for which any situation of captivity, certainly any zoo, should be required to account, explicitly and in detail. A new approach is possible to the management of elephant life in human care. A moral perspectiveelephant capabilities New thinking by Nussbaum (2006) about the moral status of animals argues that applying notions of basic justice to animals involves the concept of a life with dignity. While acknowledging that, Animals, like humans, often dont miss what they dont know, Nussbaum proposes a capabilities approach where the deep needs and abilities of an individual animal are recognized and accounted for in defining a life with dignity. This approach holds that the species norm (duly evaluated) tells us what the appropriate benchmark is for judging whether a given creature has decent opportunities for flourishing. The ethical issue in relation to any given capability is the extent to which the individual animal is harmed by being unable to exercise that capability. Great caution is required in defining harm because as humans we are strongly biased in favor of our own power interests. The capabilities approach, which begins from an ethically attuned concern for each form of animal life, offers a model that does justice to the complexity of animal lives and their strivings for flourishing. Such a model seems an important part of a fully global theory of justice (Nussbaum 2006). Applying this model to elephants, we must consider their capabilitiestheir deep needs and abilities. Field biology tells us that elephants, fundamentally, need family life: individuals should be born into families of related cows and should grow up under the care and support of a mother, female siblings and aunts. Elephants also need to live in an environment with which they can interact, having access to varied terrain and vegetation across an extensive area. Furthermore it becomes apparent that elephants should be allowed the largest measure of control over their own lives within the necessary constraints that must be imposed. They should be able to choose where in their environment to go and when, what to do when they get there, what and when to eat and drink, whom to associate with and when. This suggests that in captivity elephant training should be designed entirely to enhance elephant lives by increasing not just immediate physical security but the exercise of free choice. This moral view compels the case for a more biologically attuned approach to the management
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of elephants in zoos. Capabilities and the question of space The issue of how much space zoo elephants need in order to flourish sits at the heart of the public debate about zoo elephant welfare. Zoos have long regarded that any assessment of the biological needs of the species in their care must include consideration of enough space to house a biologically large enough sample of individuals for normal social interaction and stimulation (Curtis 1982, p. 59). Perhaps not surprisingly, given the role that tradition has played, when zoo elephants are considered, this question is often argued in isolation, again as if elephants are somehow categorically exceptional. By definition a captive animal has its needs met directly, or indirectly, through human agency. An animals needs include more than just a good diet and room in which to exercise to remain physically healthy; also included must be a host of factors affecting mental development of the individual. Again, in order to even begin to assess how an animal may be influenced by any captive environment, a careful accounting for the animals biological functioningits capabilitiesis required. How much space is required cannot be divorced from considerations of what sort of environment, overall, is required. As we have noted, Nussbaum (2006) recognizes the ethical distinction between the purpose of a capability (which may have no intrinsic ethical value) and the frustration the animal may experience if it cannot exercise this capability in some way (which may have value). The issue would seem to be how the animal experiences the world. Hediger may have anticipated Nussbaum, insofar as he reasoned consistently from the animals point of view and stated that an understanding of life in the wild was paramount (Hediger 1955, p. 12; Hediger 1969, p. 1). He considered that, generally, the quality of space provided to an animal is more important than the quantity (Hediger 1969, p. 22), a point strongly adopted by zoos (Curtis 1982, p. 59; Seidensticker & Doherty 1996, p. 187-188; BIAZA 2006). The central issue was about what the space would mean to the animal. Indeed it has been argued that if Hediger had a principal aim it was to understand the point of view of the wild animal in the zoo as an exercise in how humans and animals construct meaning (Turovski 2000, p. 308-387). For intelligent social species such as elephants, in which much of behavior and the ability to function is learned within the context of a nurturing society, any consideration of overall environmental requirements must include not only a careful consideration of how the animal will construct a coherent understanding of the world in which it lives, but also an ethical examination of just what this understanding should be. If elephants can be trained to accept conditions that are far from natural, we must ask the questions, How far is it acceptable to depart from natural conditions? How much independent agency should we foster in the individual elephant? These questions can only be answered after a careful consideration and evaluation of the characteristicsthe capabilitiesof wild elephants. Questions of sustainability A more biologically attuned approach to zoo elephants, if implemented, will have profound implications for both the way that elephants as individuals are managed and the way in which any sustainable population of zoo elephants is managed over time. Zoos are currently forced to make decisions about the amount of space provided to elephants within severe practical constraintsthe physical area of the zoo itself and the resources available for elephants. While operating within such constraints, zoo associations attach considerable importance to the notion of sustaining captive zoo populations of elephant species through time, proposing that such populations are of both indirect,
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educational value, and direct value to the overall conservation of elephant species (Standley & Embury 2004; AZA Elephant TAG/SSP 2006; Hutchins & Keele 2006, p. 223). This presents zoos with an ethical dilemma in which the interests of individual elephants must be weighed against the perceived interests of the zoo population as a whole. Zoos have recently taken some steps to try to balance these questions with, for example, decisions to move bull elephants to cows for breeding purposes rather than to separate cows for extended periods from any social grouping they may enjoy (Standley & Embury 2004, p. 54; Stevenson & Walter 2006, p. 62). From a moral perspective, Nussbaums capabilities approach to defining welfare attaches no ethical value, per se, to increasing numbers in a population of the species or to the survival of the species as a whole. Issues of justice concern harms to the species only insofar as these harms affect the individual (Nussbaum 2006). If zoo populations of elephants are to be sustainedand it is debatable that they need to be for any conservation purposeswhat does elephant biology suggest as an appropriate approach to management that will enable individual elephants to realize their capabilities and truly flourish? We might propose management based on component families of related individuals. Movement of genes between isolated groupings could indeed be almost exclusively via male elephants. The management of bull elephants in zoos would become a great deal more sophisticated. These requirements, in turn, seem logically to call for zoos to pool their resources to keep more elephants in far fewer places. These places could be located where climate is benign for elephants, obviating the need for elephants to spend extended periods of time indoors. Large areas, hundreds of acres in extent, could be provided for elephant families, where food can be grown for them, or better still, regenerated, on a rotational basis. Human resources would be devoted far less to the training and management of individuals, and more to the management of the extensive captive environment. The enrichment of elephant life could come through naturalistic social life and constant interaction with an extensive and varied environment. Finally though, zoos may need to face honestly the question of whether attempts to sustain genetically and demographically viable captive populations of elephants through time can ever be compatible with an ethical perspective of elephants as individuals. This question is particularly pertinent in North America, where analysis of the existing captive populations concludes that they cannot be sustained without further importation of individuals (Weise 2000; Hutchins & Keele 2006) and in Australasia where the establishment of a viable population of Asian elephants is configured around a limited number of bull elephants and the intensive use of artificial breeding techniques. An alternative vision An alternative vision could frame the activities of zoos from here forward in seeking to improve the welfare of the elephants they currently hold. Initially the skills zoos have developed in the training and manipulation of elephants could be applied to the task of rehabilitating existing captive elephants, wherever possible. This would involve restoring independent agency to individuals, encouraging them to build a new understanding of a more extensive and enriching social and physical environment. Such a social environment would not be naturalistic, but some groups might, over time, through births and the collective rearing of offspring, become more naturalistic in their composition and behavior. Candidate elephants might include not only those in zoos but also animals currently held in circuses or work camps in Southeast Asia. The management of bull elephants would continue to need particular attention and the requirement for younger and older bulls to interact presents a particular challenge. The entire project should be regarded as a grand
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experiment that at least might improve the lives of many zoo elephants in captivity today. The animals themselves would be challenged, stimulated and frightened (Derby, Chapter 15) at various times, but with sufficient thought and care, the outcomes would be increased independence, motivation and confidence in the individual elephants. Indeed, initially, the need for careful profiling of individual animals and deliberate planning for their future would be even more vitally important than it is under prevailing conditions. The Elephant Sanctuary in Hohenwald, Tennessee (see Buckley, Chapter 14 and http://www. elephants.com) and the Performing Animal Welfare Society (Derby, Chapter 15), provide instructive examples where some of these ideas have been formulated, and are being put into practice, particularly as they apply to cow elephants. Estimation and experimentation is applied in introducing former zoo and circus elephants that are essentially nave, and sometimes patently socially dysfunctional, to each other and to extensive areas in which they will live. The process of introduction is tailored to each individual according to its history and aims to restore independent motivation and confidence over time. This is often a long process of many small steps, the hallmarks of which are free choice, positive reinforcement and a concomitant absence of any sort of coercion. For most individuals, the process of adjustment will take the remainder of their lives. This new vision for captive elephant management essentially turns the traditional concepts of elephants in zoos on their head. The elephant enclosure is no longer an impoverished playpen occupied for a few hours a day, but an extensive living space. For humans to see elephants in such places becomes a far more special and valuable experience. The animals are presented in a context that enables them to function, as far as possible, according to species-typical patterns selected over millennia of evolution. Implementing this vision in North America would probably require no more money than the AZA says will be spent by the 40-plus institutions that plan to expand and upgrade their elephant exhibits over the next five to 10 years (AZA 2005). The provision of no more than 10 elephant sanctuaries, each of some hundreds of acres in extent, located within the more benign climatic zones of the United States, could be cooperatively established within the same time frame. Conclusions Manyand probably mostzoos are trapped in an outmoded tradition of elephant keeping, in part because of the manner in which elephants were first handled, in part because of their constrained physical locations, in part because of money. First, zoo elephants are not working elephants. Zoo elephants should be approached as wild animals and their care should be developed according to the same principles that are widely promoted by zoos as most appropriate for the husbandry of other wild species. Tradition can actually teach us little about how elephants should be treated by humans if we adopt the perspective of elephants as wild animals. Careful consideration of the capabilities of wild elephants, as described by field biologists, can help zoos adopt such a perspective. Taking this different, biological perspective will place large burdens on zoos but not ones that are insurmountable. Zoos will have to face honestly the question of whether there is really any genuine need to face the enormous challenges to effective genetic management of captive elephant populations. Current plans may not be compatible with delivery of elephant welfare, particularly social welfare. The future for zoo elephants must involve more social opportunity, more naturalistic family life, more independence and choice and, for all these things, more space. The question remains whether the practical limitations that these considerations must necessarily impose, will prevent
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zoos from establishing their own viable captive populations and demand a broader, more creative approach to the stewardship of captive populations and of wild elephants across their natural range. References

Association of Zoos and Aquariums. 2005. Top ten AZA elephant success stories: 2005 a banner year for elephants in AZA accredited zoos. Retrieved December 29, 2006, from http://www.aza.org// Newsroom/PR_Top10ElephStories/. Association of Zoos and Aquariums. 2006. Mission statement elephant taxon advisory group/species survival plan elephant. Retrieved December 29, 2006, from http://www.elephanttag.org/. British and Irish Association of Zoos and Aquariums. 2006. The welfare of zoo animals. Animal Care. Retrieved December 29, 2006, from http://www.biaza.org.uk/public/pages/care/index.asp. Broom DM. 1991. Animal welfare: concepts and measurements. J Anim Sci. 69(10):4167-4175. Clubb R, Mason G. 2002. A review of the welfare of elephants in European zoos. Horsham, UK: RSPCA. Curtis L. 1982. Husbandry of mammals. In: Sausman K, ed. Zoological park and aquarium fundamentals. Wheeling, WV: AAZPA. p. 245-255. Diamond J. 1998. Guns, germs and steel: a short history of everybody for the last 13,000 years. London,UK: Jonathan Cape. Hediger H. 1955. Studies of the psychology and behaviour of captive animals in zoos and circuses. London, UK: Butterworth Scientific Publications. (English Language translation by Geoffrey Sircom). Hediger H. 1969. Man and animal in the zoo: zoo biology. London, UK: Routledge and Kegan Paul Ltd. (English language translation by Gwynne Vevers and Winwood Reade). Hutchins M. 2006. Variation in nature: its implications for zoo elephant management. Zoo Biol 25:161-71. Hutchins M, Keele M. 2006. Elephant importation from range countries: ethical and practical considerations for accredited zoos. Zoo Biol 25:219-233. International Species Information System 2006. Abstracts. Retrieved September 29, 2006, from http://app. isis.org/abstracts/abs.asp. Lair R. 1997. Gone astray: the care and management of the Asian elephant in domesticity. Bangkok, Thailand: FAO Regional Office for Asia and the Pacific (RAP) Publication 1997/16. Lees C. 2004. Captive management plan for Asian elephant. Mosman, Australia: ARAZPA. Milroy AJW. 1922. A short treatise on the management of elephants. In: Bist SS, ed. A.J.W. Milroys management of elephants in captivity. New Delhi, India: Natraj Publishers 2002. Nussbaum MC. 2006. The moral status of animals. Chron Higher Ed 52. Retrieved March 2, 2006, from http://chronicle.com/fgree/v52/i22/22b00601.htm. Seidensticker J, Doherty JG. 1996. Integrating animal behavior and exhibit design. In: Kleiman D, Allen ME, Thompson KV, Lumpkin S, Harris H, eds. Wild mammals in captivity: principles and techniques. Chicago, IL: University of Chicago Press. Standley S, Embury A. 2004. Guidelines for management of elephants in Australasian (ARAZPA) zoos, revised first edition, December 2004. Mosman, Australia: ARAZPA. Stevenson M, Walter O. 2006. Management guidelines for the welfare of zoo animals: elephant: Loxodonta africana and Elephas maximus, 2nd ed. London, UK: British and Irish Association of Zoos and Aquaria. Sukumar R. 2003. The living elephants: evolutionary ecology, behavior and conservation. New York, NY: Oxford University Press. Turovski A. 2000. The semiotics of animal freedom: a zoologists attempt to perceive the semiotic aim of H. Hediger. Sign Sys Stud 28:380-87. Weise RJ. 2000. Asian elephants are not self-sustaining in North America. Zoo Biol 19:299-309. 107

Weise RJ, Willis K. 2004. Calculation of longevity and life expectancy in captive elephants. Zoo Biol 23:363-73.

Peter Stroud worked in major Australian zoos for 23 years, as a keeper, curator and director. From 1993 to 2003 he was active in the development of zoo elephant management in the Australasian region. He now works as an independent consultant. He is a member of the Asian Elephant Specialist Group of the IUCN Species Survival Commission. Peter may be contacted at 17 Ellen Avenue Keilor East, Victoria 3033, Australia, and pcstroud@optusnet.com.au.

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Introduction
Robert P. D. Atkinson Head of Wildlife Department The Royal Society for the Prevention of Cruelty to Animals Most professional agricultural stockmen and women would be surprised at the lack of established principles for managing elephants in zoos. They might, for instance, wonder why there is no scientifically determined optimal stocking density or universal agreement on ideal substrates or on whether or at what age a juvenile should be separated from its mother. They might question why the mortality and illness of such valuable animals seem higher than should be in a protected environment, and ask why the problem still has not been resolved. They might even inquire why zoos persist with such a demanding species, or request a look at the accounts in order to gauge the benefits against which the costs might be weighed. Many scientists and zoo managers, including the authors in this section, are starting to ask the same questions. Georgia Mason and Jake Veasey are experiencing firsthand the difficulties of assessing welfare scientifically and of making evidence-based management decisions. Joseph Barber questions the objectivity of the bases for zoo husbandry guidelines. For instance, such guidelines advise giving elephants as much space as possible, and no fewer than a certain minimum of acres. Following this guidance, zoos are building new exhibits or enhancing old ones. For example, Terry Maple and his colleagues say that there are 50 such projects in the United States alone, and that all try to incorporate more space, presumably at a cost of many millions of dollars. Yet no one really knows how much space an elephant needs. Maple and colleagues propose five acres as a minimum, but the owners of elephant sanctuaries would possibly not be happy with anything fewer than tens or hundredsand elephant field biologists, thousands. It is surely not too much to ask that zoos follow the advice of Mason and Veasey and put some of the millions they spend on exhibit design into research aimed at finding out what makes elephants healthy and happy. As Barber points out, the welfare of captive elephants is very much in the balance. The tipping of that balance must be guided by decisions rooted deep in informed compassion, and not those rooted deep in subjective opinion.

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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 welfarebased 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
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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 areoften admittedlyminimum, 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 foragingtypically 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
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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 elephants 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 todays 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
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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 facilitiesG. 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
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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
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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 communitys 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
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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 elephantsas partially recommended by the zoo guidelines reviewed hereinthen 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 environmentall 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.,
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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
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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
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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 enclosureand with that five km based on distances walked in the wild, for examplewould 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
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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 managementor the point where enough research shows that it may not be possible to care for elephants successfully in captivitywill remain unlikely. Making premature conclusions based on insufficient data may actually lead to adverse effects on the animals welfareeven 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 elephantsand 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.
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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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Couzin ID. 2006. Behavioral ecology: social organization in fission-fusion societies. Curr Biol 16(5):R169R171. Csuti B, Sargent E, Bechert U, eds. 2001. The elephants foot: prevention and care of foot conditions in captive Asian and African elephants. Ames, IA: Iowa State University Press. Dai XH, Shannon G, Slotow R, Page B, Duffy KJ. 2007. Short-duration daytime movements of a cow herd of African elephants. J Mammal 88(1):151-157. Dathe HH, Kuckelkorn B, Minnemann D. 1992. Salivary cortisol assessment for stress detection in the Asian elephant (Elephas maximus): a pilot study. Zoo Biol 11(4):285-289. Davis H, Levine S. 1982. Predictability, control, and the pituitary-adrenal response in rats. J Comp Physiol Psychol 96:393-404. Dawkins MS. 1990. From an animals point of view: motivation, fitness, and animal welfare. Behav Brain Sci 13:1-61. Dawkins MS. 1998. Evolution and animal welfare. Q Rev Biol 73(3):305-328. Dawkins MS. 2004. Using behaviour to assess animal welfare. Anim Welf 13:S3-S7. Douglas-Hamilton I, Douglas-Hamilton O. 1975. Among the elephants. New York, NY: The Viking Press. Drolet G, Beaulieu J, Mansi JA, Champagne D, LaForest S. 1995. Relationship between chronic exposure to stress and development of hypertension. Ann Endocrinol (Paris) 56:187-191 (Translation). Druce H, Pretorius K, Druce D, Slotow R. 2006. The effect of mature elephant bull introductions on resident bulls group size and musth periods: Phinda Private Game Reserve, South Africa. S Afr J Wildl Res 36(2):133-137. Duncan IJH, Wood-Gush DGM. 1972. Thwarting of feeding behaviour in the domestic fowl. Anim Behav 20:444-451. Easa PS. 1992. Movement pattern and home range of Asian elephants, Elephas maximus, in Parambikulam Wildlife Sanctuary, Kerala. In: Silas EG, Krishnan Nair M, Nirmalan G, eds. The Asian elephant: ecology, biology, diseases, conservation and management. Kerala, South India, Kerala Agricultural University. Eisenberg JF. 1981. The mammalian radiations: an analysis of trends in evolution, adaptation, and behavior. Chicago, IL: University of Chicago Press. Estes RD. 1991. The behavior guide to African mammals. London, UK: University of California Press, Ltd. Estes RD. 1999. The safari companion: a guide to watching African mammals. White River Junction, VT: Chelsea Green Publishing Co. Forthman DL, McManamon R, Levi UA, Bruner GY. 1995. Interdisciplinary issues in the design of mammal exhibits (excluding marine mammals and primates). In: Gibbons Jr. EF, Demarest J, Durrant B, eds. Captive conservation of endangered species. Albany, NY: State University of New York Press. p. 377399. Fowler ME. 2001. An overview of foot condition in Asian and African elephants. In: Csuti B, Sargent E, Bechert U, eds. The elephants foot: prevention and care of foot conditions in captive Asian and African elephants. Ames, IA: Iowa State University Press. p. 3-7. Fraser D. 1995. Science, values and animal welfare: exploring the inextricable connection. Anim Welf 4:103-117. Fraser AF, Broom DM. 1990. Farm animal behaviour and welfare, 3rd ed. London, UK: Bailliere Tindall. Freeman EW, Weiss E, Brown JL. 2004. Examination of the interrelationships of behavior, dominance status, and ovarian activity in captive Asian and African elephants. Zoo Biol 23(5):431-448. Friend TH. 1991. Behavioral aspects of stress. J Dairy Sci 74(1):292-303. Glickman SE, Caldwell GS. 1994. Studying natural behaviors in artificial environments: the problem of salient dimensions. In: Gibbons Jr. EF, Wyers EJ, Waters EJ, Menzel Jr. EW, eds. Naturalistic environments in captivity for animal behavior research. Albany, NY: State University of New York Press. p. 207-226. 124

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Gruber TM, Friend T, Gardner J, Packard JM, Beaver B, Bushong D. 2000. Variation in stereotypic behavior related to restraint in circus elephants. Zoo Biol 19:209-221. Hancocks D. 1996. The design and use of moats and barriers. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S, eds. Wild mammals in captivity: principles and techniques. Chicago, IL: University of Chicago Press. p. 191-203. Hancocks D. 2002. A different nature: the paradoxical world of zoos and their uncertain future. Berkeley, CA: University of California Press. Hatt JM, Clauss M. 2006. Feeding Asian and African elephants (Elephas maximus and Loxodonta africana) in captivity. I Zoo Yrbk 40:88-95. Hittmair KM, Vielgrader HD. 2000. Radiographic diagnosis of lameness in African elephants (Loxodonta africana). Vet Radiol Ultrasound 41(6):511-515. Hutchins M. 2006. Variation in nature: its implications for zoo elephant management. Zoo Biol 25(3):161171. Joffe J, Rawson RA, Mulick JA. 1973. Control of their environment reduces emotionality in rats. Science 180:1383-1384. Keele M. 1996. North American Asian elephant birth statistics: what are the numbers telling us. J Eleph Mgrs Assoc 7:29-32. Kirkden RD, Edwards JSS, Broom DM. 2003. A theoretical comparison of the consumer surplus and the elasticities of demand as measures of motivational strength. Anim Behav 65:157-178. Kuhar CW. 2006. In the deep end: pooling data and other statistical challenges of zoo and aquarium research. Zoo Biol 25(4):339-352. Kurt F, Hartl GB. 1995. Asian elephants (Elephas maximus) in captivity: a challenge for zoo biological research. In: Ganslosser U, Hodges JK, Kaumanns W, eds. Research and captive propagation. Furth, Germany: Filander Verlag. p. 310-326. Kurt F, Mar KU. 1996. Neonate mortality in captive Asian elephants (Elephas maximus). Z Saugetierekd 61:155-164. Lane J. 2006. Can non-invasive glucocorticoid measures be used as reliable indicators of stress in animals? Anim Welf 15(4):331-342. Laws RM, Parker SC. 1968. Recent studies on elephant populations in east Africa. In Crawford MA, ed. Comparative nutrition of wild animals. London, UK: Academic Press. p. 319-359. Leggett KEA. 2006. Home range and seasonal movements of elephants in the Kunene region, North-west Namibia. Afr Zool 41:17-36. Leong KM, Burks K, Rizkalla CE, Savage A. 2005. Effects of reproductive and social context on vocal communication in captive female African elephants (Loxodonta africana). Zoo Biol 24(4):331-347. Mason G, Mendl M. 1993. Why is there no simple way of measuring animal welfare? Anim Welf 2:301319. Mason G, McFarland D, Garner J. 1998. A demanding task: assessing the needs of captive animals. Anim Behav 55:1071-1075. McComb K, Moss CJ, Durant SM, Baker L, Sayialel S. 2001. Matriarchs as repositories of social knowledge in African elephants. Science 292:491-494. McKnight BL. 1995. Behavioral ecology of hand-reared African elephants (Loxodonta africana) in Tsavo East National Park, Kenya. Afr J Ecol 33:242-256. Meder A. 1989. Effects of hand-rearing on the behavioural development of infant and juvenile gorillas (Gorilla gorilla gorilla). Dev Psychobiol 22(4):357-376. Meller CL, Croney CC, Shepherdson D. 2007. Effects of rubberized flooring on Asian elephant behavior in captivity. Zoo Biol 26(1):51-61. Mench JA, Kreger MD. 1996. Ethical and welfare issues associated with keeping wild mammals in captivity. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S, eds. Wild mammals in captivity: principles and techniques. Chicago, IL: University of Chicago Press. p. 5-15. 125

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Mikota S, Sargent E, Ranglack GS. 1994. Medical management of the elephant. West Bloomfield, MI: Indira Publishing. Mineka S, Henderson RW. 1985. Controllability and predictability in acquired motivation. Ann Rev Psychol 36:495-529. Moss C. 1988. Elephant memories. New York, NY: William Morrow. Moss C, Poole J. 1983. Relationships and social structure of African elephants. In: Hinde RA, ed. Primate social relationships: an integrated approach. Oxford, UK: Oxford Blackwell Scientific. p. 315-325. Olson D. 2004. Elephant husbandry resource guide. Fort Worth, TX: International Elephant Foundation. Olson D, Wiese RJ. 2000. State of the North American African elephant population and projections for the future. Zoo Biol 19:311-320. Olson D, Keele M, Tuttle D. 1994. Husbandry and management. In: Mikota S, Sargent EL, Ranglack GS, eds. Medical management of the elephant. West Bloomfield, MI: Indira Publishing. p. 27-31. Olsson IAS, Westlund K. 2007. More than numbers matter: the effect of social factors on behaviour and welfare of laboratory rodents and non-human primates. Appl Anim Behav Sci 103(3-4):229-254. Owen MA, Swaisgood RR, Czekala NM, Lindburg DG. 2005. Enclosure choice and well-being in giant pandas: is it all about control? Zoo Biol 24(5):475-481. Payne K. 1998. Silent thunder. New York, NY: Penguin Books. Payne K. 2003. Sources of social complexity in the three elephant species. In: De Waal FB, Tyack PL, eds. Animal social complexity: intelligence, culture, and individualized societies. Cambridge, MA: Harvard University Press. p. 57-85. Plowman AB, ed. 2006. Zoo research guidelines: statistics for typical zoo datasets. London, UK: British and Irish Association of Zoos and Aquariums (BIAZA). Poole JH. 1994. Sex differences in the behavior of African elephants. In: Short R, Balaban E, eds. The differences between the sexes. Cambridge, UK: Cambridge University Press. p. 331-346. Poole TB, Taylor VJ, Fernando SBU, Ratnasooriya WD, Ratnayeke A, Lincoln G, McNeilly A, Manatunga AMVR. 1997. Social behaviour and breeding physiology of a group of captive Asian elephants. I Zoo Yrbk 35:297-310. Priest G, Antrim J, Gilbert J, Hare H. 1994. Managing multiple elephants using protected contact at San Diegos Wild Animal Park. In: Proc ann conf AAZPA. Wheeling, WV: AAZPA. p. 369-375. Rees P. 2001. Captive breeding of Asian elephants (Elephas maximus): the importance of producing socially competent animals. In: Hosetti BB, Venkateshwarlu M, eds. Trends in wildlife biodiversity, conservation and management. Delhi, India: Deya Publishing House. p. 76-91. Reimers M, Schmidt S, Kurt F. 2001. Daily activities and home range of Asian elephants of the Uda Walawe National Park (Sri Lanka). Abstr Int Elephant & Rhino Res Sym. Vienna, Austria. Ross SR. 2006. Issues of choice and control in the behaviour of a pair of captive polar bears (Ursus maritimus). Behav Process 73(1):117-120. Rushen J. 1991. Problems associated with the interpretation of physiological data in the assessment of animal welfare. Appl Anim Behav Sci 28(4):381-386. Rushen J. 2003. Changing concepts of farm animal welfare: bridging the gap between applied and basic research. Appl Anim Behav Sci 81(3):199-214. Sale J, Chaudhury S, Khan A. 1992. Ranging and feeding patterns of a Rajaji tusker. In: Silas E, Krishnan Nair M, Nirmalan G, eds. The Asian elephant: ecology, biology, diseases, conservation & management. Kerala, South India: Kerala Agricultural University. Schulte BA. 2000. Social structure and helping behaviour in captive elephants. Zoo Biol 19:447-459. Schulte B, Feldman E, Lambert R, Oliver R, Hess D. 2000. Temporary ovarian inactivity in elephants: relationship to status and time outside. Physiol Behav 71:123-131. Schulte BA, Freeman EW, Goodwin TE, Hollister-Smith J, Rasmussen LEL. 2007. Honest signalling through chemicals by elephants with applications for care and conservation. Appl Anim Behav Sci 102(3-4):344-363. 126

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Seidensticker J, Doherty JG. 1996. Integrating animal behavior and exhibit design. In: Kleiman D, Allen M, Thompson K, Lumpkin S, eds. Wild mammals in captivity: principles and techniques. Chicago, IL: University of Chicago Press. p. 180-190. Shepherdson DJ. 1998. Tracing the path of environmental enrichment in zoos. In: Shepherdson D, Mellen J, Hutchins M, eds. Second nature: environmental enrichment for captive animals. Washington, DC: Smithsonian Institute Press. p. 1-12. Shepherdson DJ, Carlstead KC, Wielebnowski N. 2004. Cross-institutional assessment of stress responses in zoo animals using longitudinal monitoring of faecal corticoids and behaviour. Anim Welf 13:S105S113. Sherwin CM. 2004. The motivation of group-housed laboratory mice, Mus musculus, for additional space. Anim Behav 67:711-717. Slotow R, van Dyk G, Poole J, Page B, Klocke A. 2000. Older bull elephants control young males. Nature 408(6811):425-426. Soltis J, Leong K, Savage A. 2005a. African elephant vocal communication I: antiphonal calling behaviour among affiliated females. Anim Behav 70:579-587. Soltis J, Leong K, Savage A. 2005b. African elephant vocal communication II: rumble variation reflects the individual identity and emotional state of callers. Anim Behav 70:589-599. Standley S, Embury A, eds. 2004. Guidelines for management of elephants in Australasian (ARAZPA) zoos. Proboscid and Perissodactyl Taxon Advisory Group, ARAZPA. Stevenson MF, Walter O, eds. 2006. Management guidelines for the welfare of zoo animals: elephants Loxodonta africana and Elephas maximus, 2nd ed. London, UK: British & Irish Association of Zoos & Aquariums. p. 217. Stoinski TS, Hoff MP, Lukas KE, Maple TL. 2001. A preliminary behavioral comparison of two captive all-male gorilla groups. Zoo Biol 20(1):27-40. Stoinski TS, Lukas KE, Kuhar CW, Maple T. 2004a. Factors influencing the maintenance and formation of all-male gorilla groups in captivity. Zoo Biol 23(3):189-203. Stoinski TS, Lukas KE, Kuhar CW, Maple TL. 2004b. Social dynamics of captive western lowland gorillas living in all-male groups. Behav 141:169-195. Stricklin WR, de Bourcier P, Zhou JZ, Gonyou HW. 1998. Artificial pigs in space: using artificial intelligence and artificial life techniques to design animal housing. J Anim Sci 76(10):2609-2613. Sukumar R. 2003. The living elephants. New York, NY: Oxford University Press. Swaisgood RR, Shepherdson DJ. 2005. Scientific approaches to enrichment and stereotypies in zoo animals: whats been done and where should we go next? Zoo Biol 24(6):499-518. Swaisgood RR, Ellis S, Forthman DL, Shepherdson DJ. 2003. Commentary: improving well-being for captive giant pandas: theoretical and practical issues. Zoo Biol 22(4):347-354. Taylor VJ, Poole TB. 1998. Captive breeding and infant mortality in Asian elephants: a comparison between twenty western zoos and three eastern elephant centers. Zoo Biol 17:311-332. Todman JB, Dugard P. 2001. Single-case and small-n experimental designs: a practical guide to randomisation tests. London, UK: Lawrence Erlbaum Associates. Veasey J. 2006. Concepts in the care and welfare of captive elephants. IZY 40:63-79. Vinod T, Cheeran J. 1997. Activity time budget of Asian elephants (Elephas maximus) in Idukki Wildlife Sanctuary, Kerala, South India. Indian Forester 123(10):948-951. Volodina E, Volodina I. 1999. Bioacoustics in zoos: a review of applications and perspectives. Int Zoo News 4:208-213. Warburton H, Mason G. 2003. Is out of sight out of mind? The effects of resource cues on motivation in mink, Mustela vison. Anim Behav 65:755-762. Webster AJF, Knott L, Tarlton JF. 2005. Understanding lameness in the dairy cow. Cattle Pract 13:93-98. Weisz I, Wuestenhagen A, Schwammer H. 2000. Research on nocturnal behaviour of African elephants at Schnbrunn Zoo. Int Zoo News 47:228-233. 127

West G. 2001. Occurrence and treatment of nail/foot abscesses, nail cracks, and sole abscesses in captive elephants. In: Csuti B, Sargent E, Bechert U, eds. The elephants foot: prevention and care of foot conditions in captive Asian and African elephants. Ames, IA: Iowa State University Press. p. 93-97. Wiedenmayer C, Tanner R. 1995. Untethered housing of Asian elephants at Zrich Zoo. I Zoo Yrbk 34:200205. Wielebnowski N. 2003. Stress and distress: evaluating their impact for the well-being of zoo animals. J Am Vet Med Assoc 223(7):973-977. Wielebnowski N, Busso JM, Brown JL. 1999. Adrenal activity in relation to subjective temperament assessment in clouded leopards (Neofelis nebulosa). In: Wildt DE, Mellen JD, Brown J, eds. Felid TAG action plan. Annual report. Lake Buena Vista, FL: AZA, Disneys Animal Kingdom. p. 74-75. Wielebnowski NC, Fletchall N, Carlstead K, Busso JM, Brown JL. 2002. Noninvasive assessment of adrenal activity associated with husbandry and behavioral factors in the North American clouded leopard population. Zoo Biol 21(1):77-98. Wilson ML, Bloomsmith MA, Maple TL. 2004. Stereotypic swaying and serum cortisol concentrations in three captive African elephants (Loxodonta africana). Anim Welf 13(1):39-43. Wyat JR, Eltringham SK. 1974. The daily activity budget of the elephant in the Rwenzori National Park, Uganda. E Afr Wildl J 12:273-289.

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 Disneys 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 joseph@barberconsulting.org.

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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 cant 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 elephants 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 surroundingsnatural 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 Sommers 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. Sommers (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 zoos 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 Aquariums (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). AZAs 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).
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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 Seattles 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 Parks 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 Atlantas 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 exhibits debut in 1988. Atlantas 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 1990s, 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) Childrens Zoo
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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 zoos 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 Atlantas 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
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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.
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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. Disneys 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
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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 Howletts 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 associations 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. AZAs 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. Disneys 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
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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 exerciseand 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 elephants 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
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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
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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
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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 elephants 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 AZAs 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 elephants 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.
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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
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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
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decisions about when to intervene medically. It may also be useful to consider Maslows 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 animals 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 earths 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
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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 elephants 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, AZAs 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,
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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. Bloomsmiths 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. Martins 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. Maples 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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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 Terry.Maple@msn.com; 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 mabloom@emory.edu. Allison L. Martin is a graduate student in the School of Psychologys 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 Allison.martin@gatech.edu.

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Georgia Mason Canada Research Chair in Animal Welfare, Animal Science Department University of Guelph and Jake S. Veasey Head of the Department of Animal Management and Conservation Woburn Safari Park The welfare of elephants is an enormous challenge for zoos in terms of animal husbandry, financial cost and public perception. This chapters aim is not to discuss whether elephants should be held in captivity: resolving this issue would involve sound data on the costs and benefits of keeping them in zoos, and reconciling the diverse ethical beliefs of different people. Instead, we review how animal welfare is assessed scientifically; discuss what is known about these various techniques for elephants; survey the evidence concerning population-level welfare of elephants in zoos; summarize the possible causes of reduced welfare amongst captive elephants; review the (disturbingly sparse) information that has been collated to test some of these ideas; and discuss what future work is needed to objectively evaluate the psychological welfare of zoo elephants. What do we mean by welfare and how can we measure it? Animal welfare relates to an animals affective state: what it feels. Good welfare thus means experiencing positive emotional states and negligible suffering, while poor welfare entails severe or prolonged states of mental suffering (e.g., Dawkins 1990; Mason & Mendl 1993). To augment this definition, we should clarify what welfare is not. First, health and welfare are distinguishable. Although health can obviously affect welfare (and welfare can affect health, as we review below), health typically refers to physical, not psychological, well-being. Thus, if a disease causes pain, or reduces an animals ability to behave normally, it may well reduce welfare; however, an ailment that does not influence behavior or stimulate pain receptors (e.g., a tumor that the animal cannot feel) does not necessarily affect welfare, at least at that time. Second, welfare is not about simple genetic fitness, i.e. the extent to which an individual increases the frequency of its genes in subsequent generations. While poor welfare can decrease reproductive output, this is not always the case. It would be incorrect, for example, to assume that highly selected livestock that are managed intensively have acceptable welfare simply because they are reproducing. Third, good welfare is not about mimicking all aspects of natural life. Performing some natural activities may be important for an animals welfare, but others may be harmlessly eliminated when human provisioning and protection render them obsolete (e.g., Veasey, Waran & Young 1996a). Furthermore, life in the wild can,
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as Hobbes put it, be nasty, brutish and short; the behavioral repertoire, health status and lifespan of free-living animals thus do not automatically yield high welfare benchmarks (see also Veasey et al. 1996a: Veasey, Waran & Young 1996b). Finally, death per se must be differentiated from welfare. The manner in which an animal dies, and the factors precipitating its death, are relevant to welfaresince the processes involved may have caused suffering. However, because death involves the cessation of brain activity (which eliminates the possibility of suffering), and because death can be humane (the aim of euthanasia by definition), loss of life per se need not imply poor welfare. If welfare is about how an animal feels, then in the absence of a common language, how do we investigate it? The subjective experiences, thoughts and feelings of an individual animal are inaccessible (the so-called Other Minds problem), and so to assess them we need indirect indicators of psychological well-being. When evaluating welfare in other humans, we use learned verbal or sign language, as well as innate body language (smiling, crying, grimacing, etc.), whose affective correlates we understand from our own experiences and behavior. In general, these indices serve us wellbut they can be challenging and potentially unreliable in some cases: for example, for premature and neonatal infants, the profoundly physically disabled and people with disorders like psychopathy. In such instances, physiological indices may be used, such as changes in heart rate, skin conductivity or endocrine and immune responses validated as correlates of distress. Similar challengesperhaps even greater onesare faced when evaluating welfare in other species. We have to interpret alien signals (ear-flapping, growling, etc.); we may well need indices of physiological functioning; and we must interpret all our findings without anthropomorphism, bias or circular reasoning. Overall, we have to recognize that we can never be certain about the conscious experiences of other beings, although assuming that they do exist is a precautionary principle used by most. As a result, what are commonly referred to as welfare measures are, in fact, welfare indicators from which we can only make inferences. But what exactly are these indices and where do they come from? Most have their historical origins in two well-established fields of science: clinical research into humans with physical or mental problems, and experimental animal-based physiology and neuroscience research. The relevant human clinical research involves work on suffering people: individuals going through stressful events like divorce, bereavement, war or exams; experiencing emotional disorders such as anxiety and depression; or experiencing physical harm that causes pain or nausea. These individuals verbal reports of their subjective experiences can be compared with changes in their biological functioning (e.g., hormonal profiles), to glean potential indices of mental state. The second type of research to generate welfare indices has been fundamental work in which research animals (typically rats, mice and primates) are exposed deliberately to events believed to cause fear, sickness or pain. Some relevant work also experimentally mitigates suffering via analgesic drugs, anxiolytics or anti-depressive agents. Behavioral and physiological changes seen in these animals are, again, potential indices of the emotional state assumed to be caused or redressed by those stimuli. Reassuringly, indices from both these broad fields tend to indicate similar responses for use in welfare assessment. Next we review what these indices are and how they might be used to gauge the welfare of elephants in captivity. How to assess elephant welfare? Below we review several stress and welfare texts (e.g., Archer 1979; Dawkins 1980, 1990; Mason & Mendl 1993; Broom & Johnson 1997; Toates 1997; see also Clubb & Mason 2002, p. 7) to extract some key welfare indices. Note that in welfare research on other animals (e.g., agricultural
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species), such indices are most often used to assess aspects of husbandry such as enclosure size, stocking density and so on; findings are typically then used to generate general, population-wide recommendations (which might not be implemented until long after the research animals yielding the relevant data are dead). In zoos, however, such an approach may be both difficult (an issue we return to later), and even inappropriate: the individuals under study are typically the very objects of concern, not merely exemplars of their species. Happily, welfare indices can be used to investigate individual differences within a population, thus identifying influential aspects of the environment, genotype or past experience that render individuals either particularly vulnerable or impervious to certain welfare challenges; and furthermore, by applying these indices to known individuals, work can also be carried out with the specific aim of improving the immediate welfare of these particular individuals on a case-by-case basis. Below, we summarize indices that are particularly sensitive to psychological welfare, i.e. to stress, frustration and anxiety, or fear. For brevity, we sidestep indices of problems caused by physical disease or injury (and note too that the list below is not exhaustive). In each section we summarize what species-specific knowledge we have of these indices for use with zoo elephants. We cover first behavioral and psychological changes, then physiological changes and, finally, the consequences of physiological changes for reproduction and physical health. Behavioral and psychological changes Behavioral changes and the processes in the brain that drive them (e.g., assessment, decisionmaking and learning) are at the heart of animal welfare assessment because they are so intimately connected with pleasure, pain and other feelings. Indeed, the very reason that animal welfare causes concern, while plant welfare does not, is because animals move, forage and perform a range of other activities in which emotions have seemingly evolved to play a key controlling role. Preference and avoidance Stimuli or resources that decrease welfare are typically avoided, via both learned and unlearned behavioral responses; stimuli or experiences that increase welfare are typically sought out, again via unlearned responses (like approach), and learned ones such as moving to specific locations associated with the presence of reward (conditioned place preference) or performing an arbitrary task to gain it (e.g., rats learning to lever-press). The more important a resource is to fitness and welfare, the more effort animals are likely to allocate to gaining it: thus animals typically work harder (travel farther, overcome greater obstacles, lever-press longer, etc.) for food and water than they do for non-essential resources, and they do so more after deprivation than when satiated. Such behavioral responses are inextricably tied up with the emotional value of different stimuli and experiences: some argue that the function of emotions is to control motivation (the goal-directed, effortful aspects of behavior) and promote learning (e.g., Cabanac & Rolls as reviewed by Dawkins 1990). Preference tests have therefore been used to reveal what animals would choose in order to secure better welfare. For example, chickens will choose larger cages with a substrate, compared to smaller cages with a wire floor (Dawkins 1980), while naturally semi-aquatic American mink will push door-weights as heavy as those they will push to gain food, in order to reach water in which they can perform natural swimming and head-dipping activities (Mason, Cooper & Clarebrough 2001). Negative stimuli can be assessed too, such as animals avoidance of noxious gasses, or aspects of being transported by truck (e.g., physical vibration: Cooper, Mason & Raj 1998; Jones, Wathes & Webster 2003; MacCaluim, Abeyesinghe, White & Wathes 2003). Nor are techniques like these restricted to assessing attributes of the environment; lame poultry will choose food dosed with
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analgesics over unadulterated food, thus showing that they are sensitive to the analgesic effect and seek it out, and therefore must have been experiencing pain (e.g., Danbury, Weeks, Chambers, Waterman-Pearson et al. 2000). Overall, identifying whether stimuli or experiences induce learning, and assessing the efforts animals put in to reach or avoid them, can therefore be very useful for identifying and ranking factors that increase or decrease welfare. Issues to be aware of when using such data include the fact that animals may need a period of time to experience and learn about the positive or negative effects of the stimuli on offer. In addition, preference data may need interpretation: threatening stimuli can elicit an approach response due to animals need to gain information about potential danger (e.g., predator inspection by prey species); and, furthermore, when animals interact with a rewarding resource, the stimuli elicited by it (its sounds, odors, etc.) and experience gained by interacting with it, may enhance or even create a motivation for itwithout such effects, out of sight could well have been out of mind. Thus, preference for enrichments typically indicates the benefits of adding them to an enclosure, and the welfare implications of then removing them; but it does not necessarily indicate suffering in animals that have never experienced such enrichments at all (Warburton & Mason 2003). Measures of preference and avoidance are likely to be as relevant and useful for elephants as they are for other animals. For example, studies of wild elephant ranging behavior has been used to quantify their avoidance of areas of human disturbance, seen even when these humans are merely groups of harmless (albeit obstructive) tourists on safari (Slotow 2002; Blom, van Zalinge, Mbea, Heitkonig et al. 2004). Satellite tracking has also demonstrated that African elephants avoid walking uphill (Wall, Douglas-Hamilton & Vollrath 2006). In zoos, studies of preference have been little used as yet (Mellor, Croney & Shepherdson 2007 give one preliminary example). However, preference data could potentially be very useful. For example, an experiment in which elephants could choose between two identical overnight pens, one in which they would be chained, one in which they would not be, could be used to tackle the question Do zoo elephants dislike being shackled at night? Preference experiments could also be designed to address the question Do elephants find some keeper contact rewarding? and many other topical welfare issues. Other behavioral measures related to preference, avoidance and other motivations Animals tendencies to avoid threatening stimuli can be used in a quite different way in welfare assessment. For one, avoidance responses (e.g., startle) can be of value for assessing an animals state, not just for quantifying the aversiveness of particular stimuliwith increased tendencies to avoid a known, standardized threatening stimulus reflecting underlying anxiety. We review this in more detail in the following section. In addition, high levels of frustrated motivation, such as a thwarted desire to approach or avoid stimuli, or thwarted motivations to engage in other activities, can also cause other changes in behavior that are useful in welfare assessment. These comprise intention movements, where animals attempt to reach a relevant resource despite repeated failure; redirected activities, where animals use inappropriate stimuli as outlets for their motivation (e.g., mating with an inanimate object); and displacement activities, where a conflict between two strong but incompatible motivations causes an animal to perform irrelevant activities like brief grooming movements. These responses can thus help reveal an animals state. Furthermore, if repeated and sustained, these responses can give rise to stereotypic behaviorsabnormal behaviors that we review in more detail below. Free-living elephants seem to show many examples of intention and displacement activities. In the ElephantVoices Signals database for African elephants (see http://www.elephantvoices. org), these include trunk twisting or foot swinging, often seen when elephants are unsure of what
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action to take; and displacement grooming, often seen when elephants have the competing motivations to both fight and flee. Shuffling back and forth (as well as swinging one leg) have also been described anecdotally for African females caught between wanting to defend their calves and being frightened of a threat (Masson & McCarthy 1994, citing work by Moss). Such indices seem not, however, to have been used in studies of captive elephant welfare, with the possible exception of stereotypic swaying (see below). Startle and other responses to ambiguous, potentially threatening stimuli Many tests of anxiety, especially those conducted on rodents to research anxiety disorders and their treatment, involve exposing an animal to a stimulus that is inherently mildly aversive, and observing its reaction. Such stimuli include open, brightly lit areas or novel objects/foods, which rodents typically avoid, especially at first. Importantly, such avoidance responses are strongest in individuals exposed to prior treatments that increase their anxiety levels (e.g., social isolation). Another innate avoidance response used to test for anxiety is a startle response that can be induced by a sudden sound or touch; again, animals previously exposed to stressful experiences such as isolation or predator cues show more exaggerated startle responses than those without comparable exposure. These anxiety indices are standard in biomedical research (see e.g., Crawley 2000), have recently come to be used in rodent welfare research and have also just started to be used on other animals, for example agricultural hoofstock. In contrast, their use to address zoo animal welfare questions has been negligible, with no known application to elephants as yet. However, it is notable that in the ElephantVoices Signals database, signs of apprehension include the fearful body-jolt, a sudden jerk of the body away from a frightening sound or movement, suggesting that startle magnitude could be a useful index of elephant anxiety. Caveats in the use of all these avoidancerelated measures include that they are more sensitive to some welfare problems (e.g., anxiety, fear) than to others (e.g., hunger, pain). Signs of increased vigilance such as head-up scanning postures, or eye widening, may be used as welfare indicators. For example, eye widening, as manifest in eye-white exposure, has been well validated as a fear/distress index for cattle (e.g., Sandem 2002). Opening the eyes wide to show the whites has similarly been reported in wild African elephants that are alarmed, frightened or engaged in intense social interactions and excited play (Poole 1996, cited in the ElephantVoices Signals database). This suggests that, with the caution that one should control for high general arousal, eye white could be useful in elephant welfare assessmentboth to identify negative stimuli and, via the use of standardized probe stimuli, to assess underlying levels of anxiety. Signals to conspecifics Social animals, and mothers and infants, often signal to each other about events of emotional significance, particularly to warn of danger, and also seemingly to convey relaxation and social contentment (e.g., the purring of cats). The use of such responses in welfare assessment needs to be validated for each species on a case-by-case basis. Good examples in welfare or stress research include vocal pain responses in piglets (Weary, Braithwaite & Fraser 1998) and chromodacryorrhoea, a red tear-like secretion thought to contain pheromones, in laboratory rats (Mason, Hampton, Wilson & Wrbel 2004). Caveats in the use of signals include: the dangers of anthropomorphic responses to signals that look like our own (e.g., liquid running from the eyes); that humans are insensitive to many animal signals, such as odors, or sounds made at frequencies that our ears cannot detect; and that signals typically indicate specific problems, not all problems (thus an absence of vocalizations
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indicating predator threat, for example, does not mean an animal has no welfare problems). Those working directly with wild elephants report many signals to conspecifics that seem emotionally significant, including a diverse range of trunk and ear postures (the ElephantVoices database once again includes many examples). The flow of liquid (temporin) from the temporal glands has also anecdotally been linked with excitement and high arousal, including stressful situations; Slotow (2002) even suggests that it flows when wild elephants are disturbed by humans, though not all report this and most interpret it as a social signal (e.g., Weibull & Eriksson 1998) especially as it is most marked during musth (Sukumar 2003). Postural and other conspicuous signals are no doubt used in an informal, everyday way by experienced and perceptive elephant keepers, and indeed by the mahouts of working Asian elephants. However, their potential usefulness in and formalized application to welfare assessment seems not to have been developed. Note that it is likely that not all social signals of warning, fear or distress in elephants can be detected readily by humans, especially those involving infrasound (anecdotally, African elephants have displayed signs of fear when conspecifics many kilometers away have been alarmed, possibly by detecting their infrasonic vocalizations: Masson & McCarthy 1994). Negative cognitive bias Humans in a negative mood state or with depression (see below) show pronounced alterations in how they perceive and classify events; in particular, neutral or mildly negative events are reported as being more negative or threatening than they are by humans in a positive mood state. Recent research has shown that similar cognitive biases seemingly occur in animals. Rats were trained that if they heard a sound at a certain pitch, food would be delivered if they pressed a lever, but if they heard a sound of another pitch, the lever would not deliver food, and instead would emit a blast of aversive white noise (Harding, Paul & Mendl 2004). These trained rats were housed in two waysin large cages full of rewarding enrichments, or in standard cages made stressful by regular disruption. The two groups were then exposed to the two sounds againas well as a range of control sounds of intermediate pitch. The rats housed in enriched versus stressful environments differed in their response to these ambiguous sounds. Enriched rats treated intermediate sounds as though likely to predict a lever-delivered treat, while stressed rats, in contrast, were more pessimistic, acting as though there were a low chance of reward. Such methods of quantifying negative cognitive bias are still in the process of being refined and fully validated, and thus have not yet been used on zoo animals. However, in the future they could be ideal for doing so, especially for species like elephants whose learning abilities should make training in the relevant tasks quite easy. Abnormalities in behavior and brain function I: apathy and depression-like changes As well as negative cognitive bias, humans with depression reduce their performance of activities that require motivation or usually cause pleasure, e.g., personal care, work, exercise, social interaction and sexual activity. Similarly, low levels of activity and reduced libido are often observed in rodents subject to repeated stressors, and indeed such stressful treatments are often used to model depression in biomedical research. Low levels of activity, poor self-grooming, low libido and a lack of interest in maternal care are often observed in captive animals. Sometimes labeled apathy, these changes are disturbingbut, typically, it is hard to classify them with confidence as depression-like. Validation would include looking for negative cognitive bias (see above) or for alterations in certain endocrine systems (see the HPA axis, below); and using antidepressants to see if these reverse the observed effects.
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Such cautions firmly in mind, there have been strikingif anecdotalaccounts of elephants becoming intensely quiet and inactive, especially after social separation (Masson & McCarthy 1994). Similarly, ill elephants have been said to move their trunks, switch their tails and flap their ears far less than healthy animals (Chatkupt & Sollod 1999, citing Schmidt 1986). Indeed, one survey of Thai working elephants (Chatkupt & Sollod 1999) used the degree of body movement to assess welfare. Elephants that moved intermittently were found to have poorer body condition than those that moved frequently; animals described as dull or quiet were also more likely to have poorer body condition. While such categorization was rather subjective, and confounding variables abounded in this study (for example, poor body condition and little movement both occurred more in shady conditions), attempts to use such behavioral indices could prove useful in future studies. Abnormalities in behavior and brain function II: stereotypies and other repetitive behaviors Abnormal repetitive behavior, such as stereotypic pacing, is common in zoo animals (e.g., Mason, Clubb, Latham & Vickery 2007), and has long been used in welfare assessment. The rationale for this is two-fold: it often originates from behavioral signs of high, frustrated motivation (see above); and it is typically caused by environments that induce other signs of poor welfare (e.g., other indices reviewed here; see also Mason & Latham 2004; Mason 2007a; Mason et al. 2007). Indeed, stereotypic behaviors have been formally defined as repetitive behaviors induced by frustration, repeated attempts to cope and/or central nervous system (brain) dysfunction (Mason 2007a). As with all welfare indices, they are not perfect. Some repetitive behaviors seem innocuous with respect to welfare (e.g., a toddler sucking a pacifier or a cat kneading on a lap); and, often, we simply do not know the biological cause of repetitive behavior in zoo animals. A second caveat is that some stereotypic behaviors may indicate past welfare problems more than present, for instance if they reflect abnormal brain development during infancy (Mason & Latham 2004; Mason 2007b; Mason et al. 2007). A third caveat is that, whether groups or individuals with little stereotypic behavior have better welfare than those displaying high levels depends on what they are doing instead: if those with low rates of stereotypic behavior are instead apathetic (see above), hiding or comparatively immobile due to pain (e.g., Mellor, Croney & Shepherdson 2007), their welfare may actually be poorer than that of animals with overt abnormal behavior. Common examples of abnormal repetitive behavior in zoo elephants include swaying/weaving, head-nodding and sometimes pacing (see Clubb & Mason 2002). Because at least some forms are increased by treatments like tethering (e.g., Friend 1999; Kurt & Gara 2001) or stressful experiences like the onset of parturition (Szdzuy, Dehnard, Strauss, Eulenberger et al. 2006), it seems reasonable to class them as true stereotypic behaviors. In one recent survey of 29 individuals in five zoos, side-to-side swaying/weaving was the most common form. Performance of weaving/swaying increased with age, and females performed these behaviors more than males (Quaid, Harris, Harris & Sherwin 2006). Stereotypic behavior typically does not seem time-consuming in zoo elephants (e.g., Clubb & Mason 2002; Harris, Harris & Sherwin 2006). However, it is prevalent: although reported at low rates, it is found in a large proportion of the population (40 percent; Clubb & Mason 2002). Zoo elephants are less prone to stereotypic behavior than are circus elephants (Clubb & Mason 2002). However, they are certainly more prone than wild elephants: although transient swaying has been observed here (see above), such behaviors, when they do occur, occur far less frequently than in captivity.

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Physiological responses and their consequences Behavioral and cognitive responses to threats or stressors are supported (e.g., fuelled) by appropriate changes in underlying physiology. Many of these necessary, adaptive changes in organ function, cellular responsiveness and metabolic rates underlie the common stress responses with which we are all familiar: racing hearts, dilated pupils and so on. Such changes are very useful as welfare indices, although like some of the behavioral responses previously discussed, they can suffer from poor specificity because they may be elicited by all situations of activation or excitement, including positive ones. If activation is prolonged or excessive, some of these physiological responses change and either habituate or sensitize; adaptive side effects can occur, such as hypertrophy of the organs involved; and harmful side effects can also occur, such as poor growth rates or compromised abilities to resist disease (changes that we review in a later section). Adrenaline and sympathetic nervous system responses The release of adrenaline (epinephrine) and noradrenaline into the bloodstream is part of the sympathetic responsea suite of neural and hormonal changes that help animals optimize the performance of behaviors that need energy, such as fleeing or fighting. Sympathetic activation causes the effects most of us will know from personal experience: increased heart and respiration rates, pupil dilation, urination and defecation and a measurable increase in skin conductance caused by sweating. All of these are common effects of acute stress or fear; and in humans with chronic anxiety, such responses may be elevated for long periods of time. In animal studies, especially in rodentbased research, defecation rates are often used as indices of acute anxiety, while heart rate is often measured in studies of fear, either via implanted devices or strap-on external heart-rate monitors. Furthermore, adrenaline and noradrenaline can be detected in saliva and urine; these non-invasive ways of detecting events in the plasma minimize risks that the sampling method itself will elevate the hormones being measured. The main caveat when using such indices in welfare assessment is that they are also sensitive to pleasurable behavioral activation, such as playing or copulation. In terms of using the sympathetic responses of elephants in welfare assessment, adrenaline and noradrenaline levels can be assayed from urine (Dehnhard 2007), and adrenaline can also be extracted and assayed from elephant saliva (Exner & Zanella 1999). To date these hormones seem to have been investigated in zoo animals only, so there are no data from free-living animals to provide a reference. Skin conductance measures are only valid for species with glandular skin, so are unlikely to yield useful data for elephants. Measures like urination and defecation rates, pupil diameter and heart rate, in contrast, have great potential value for elephant welfare assessment, yet seem not to have been used. The hypothalamic-pituitary adrenal axis I: corticosteroid levels For physiologists, the hypothalamic-pituitary adrenal (HPA) axis is the classic stress system of the body. It involves glucocorticoids being secreted by the adrenal gland, in response to the release of adrenocorticotrophic hormone (ACTH) by the brains pituitary gland. Glucocorticoids are hormones that facilitate the mobilization of energy reserves to prepare the animal for a response such as fight or flight. They are secreted during an animals normal activity periods (thus showing a circadian pattern in many species), but are also elevated by exposure to aversive stimuli. They thus complement sympathetic responses, but typically are activated for longer after a threat and have more diverse secondary effects on other physiological processes throughout the body. Assessment of HPA activity in animal welfare work involves measuring ACTH and corticosteroids in the plasma, or corticosteroids that diffuse into the urine or saliva (as with adrenaline,
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peaks track peaks in the plasma, while being easier to collect without causing sampling stress), and corticosteroid metabolites evident in the feces. Techniques have also been developed recently to assay corticosteroids laid down in the follicle during hair/fur growth (e.g., Davenport, Tiefenbacher, Lutz, Novak et al. 2006). Like sympathetic responses, HPA responses sometimes have to be treated with caution because acute elevations in glucocorticoids can occur during excitement or simple exertion rather than in situations where welfare is compromised. In elephants, cortisol is the key corticosteroid produced by the adrenal gland. Baseline levels, or rapid, brief elevations of cortisol output, may be detected in both elephant saliva (Dathe, Kuckelkorn & Minnemann 1992; Exner & Zanella 1999) and urine (Brown, Wemmer & Lehnhardt 1995). Baseline levels and longer, more sustained changes in output, may also be detected via metabolites in the feces (Wasser, Hunt, Brown, Cooper et al. 2000; Foley, Papageorge & Wasser 2001; Ganswindt, Palme, Heistermann, Borragan et al. 2003; Hunt & Wasser 2003 for Africans; Millspaugh 2003; and, e.g., Laws, Ganswindt, Harris, Harris et al. 2007 for Asians). These metabolites peak in the feces approximately 30 hours after a stressful event. Validation of these fecal assay techniques in wild elephants includes their increase with natural stressors like being a subordinate herd member, or being exposed to severe dry seasons (Wasser et al. 2000; Foley, Papageorge & Wasser 2001); they also co-varied with submissive behavior in one study of zoo elephants (Burks, Mellen, Miller, Lehnhardt et al. 2004). Intriguingly, 13 zoos recently surveyed across the UK were found to differ significantly in the mean levels of such metabolites in their elephants feces (Harris et al. 2006). There may now be enough published data to compare zoo and wild outputs, at least for African elephantsalthough this task should only be done by someone knowledgeable about assay techniques and how they may affect results (Touma & Palme 2005). Some specific findings from zoo studies are outlined in a later section. A final assay technique with untapped but enormous potential is to quantify cortisol trapped in hair. If cortisol extraction techniques were validated for elephant hair, we could use the long hairs from their tails to assess the impact of events throughout the previous year, which would be extremely useful for the retrospective investigation of past experiences. Assaying hair steroids to infer the time line of significant past events has thus long been used in human drug-testing, thanks to the serial deposition of such compounds along the hair shaft (see Davenport et al. 2006). Furthermore, research in a quite different field has shown that certain isotopes deposited in freeranging elephants tail hairs reliably reflect their movements and diets over the previous 12 months (Cerling, Wittemyer, Rasmussen, Vollrath et al. 2006). The hypothalamic-pituitary adrenal axis II: changes in HPA functioning In cases of chronic stress, HPA outputs and responsiveness can be chronically elevated; this can even result in the hypertrophy of the adrenal gland cortex (e.g., Terio, Marker & Munson 2004 on cheetahs). The HPA system can also respond with changes in circadian patterning (the loss of the normal night-time trough is a feature of some humans with depression) or even decrease in adrenal activity, largely due to habituation of the adrenal gland to ACTH. Thus, while chronic elevation is a likely sign of severe welfare problems, unchanged or even reduced activity may also occur, making interpretation complex and in need of validation by other measuresparticularly ACTH levels, signs that any chronic changes in HPA function have caused lasting harm (see below) or independent welfare indices (e.g., those reviewed elsewhere in this chapter). Long-term studies of HPA output or changes in circadian patterning seem not to have been conducted on zoo elephants; and although elephant adrenals have been well-studied (Kramer, Teixeira & Hattingh 1991) and are typically removed during necropsies (cf. AZA standard protocols), there also seems
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to have been no use of elephant adrenal size/structure post mortem to assess the merits or demerits of particular husbandry systems. Negative effects of prolonged physiological stress If stress is chronic, health and fecundity may be affected. Consequences of chronic physiological stress include immuno-suppression, poor wound healing, reduced fertility, reduction in protein synthesis (e.g., body-mass loss), elevated blood pressure, gastric ulceration, thickening of the arteries and premature death. These result partly from the direct effects of over-activation of the endocrine systems involved (e.g., on reproductive physiology and inflammatory pathways), and partly from less effective immune responses to pathogens. Increased morbidity and decreased lifespan In humans, stress is well documented to cause increased susceptibility to both opportunistic infections (e.g., oral and gastric ulcers, fungal infections, skin boils and Herpes sores) as well as to infectious diseases caught from conspecifics (e.g., colds and influenza). The same effects can be seen in a range of other species (cf. Mikota, Chapter 6). Recovery rates, including the repair of damaged tissues, also decline. Isolating social rodents can impair wound healing, for example (Detillion, Craft, Glasper, Prendergast et al. 2004). Although they can sometimes be complex to interpret (for example, do increased disease rates indicate compromised defenses against parasites, or merely chance exposure to more pathogens?), these potential consequences of chronic stress can be useful in assessing animal welfare, not least because they may cause as well as reflect poor welfare. Because stress increases both infectious and non-infectious disease, chronic stress also decreases lifespan in species as diverse as rats, humans and rhesus monkeys (reviewed by Clubb, Lee, Mar, Moss et al. subm.), the typical pattern seemingly being that stress shortens mature adult lifespan (e.g., KiecoltGlaser, McGuire, Robles & Glaser 2002; Cavigelli, Yee & McClintock 2005). As ever, there are constraints on the usefulness of lifespan to infer welfare, not least that it can be affected by a host of other variables, some of which, like access to ad lib. food, may even be positive for psychological welfare. However, despite this caveat, premature adult death could, if used carefully, be a particularly useful welfare indicator for zoo animals because they are frequently allowed to reach maximal longevity (even if there is terminal veterinary intervention). So, what relevant work has been done in elephants? Foley and co-workers (2001) found a correlation between conspicuous signs of gastro-intestinal parasitism and corticosteroid levels in wild African elephants. This would be consistent with a link between stress and increased vulnerability to parasitism (although it could equally indicate an increase in stress as a result of a parasitic infestation). In zoo elephants, considerable welfare concern has been raised by their apparently high rates of skin infections and lameness. Much of this may be due to enclosure substrates that do not optimize skin and foot condition, but the possible role of stress-related immuno-suppression has been little discussed in the zoo community (cf. Clubb & Mason 2002) and certainly not investigated, either in terms of underlying biological mechanisms or via correlations with other welfare indices. However, in one recent survey of 16 zoo elephants, lameness scores co-varied with fecal corticosteroid metabolite outputs, with the lamest animals showing the greatest endocrine signs of stress (Rajapaksha, Harris, Sherwin & Harris 2006). This could be consistent with stress playing a role in the underlying causes of some foot problems (although it could equally reflect that pain and disability cause stress to these animals). Welfare concernas well as much controversyhas also been raised by apparently short lifespans in zoo elephants (cf. Clubb & Mason 2002). For example, survivorship curves in Kurt
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(1995) for female Asian elephants show median lifespans of c. 33 years for Burmese working animals, c. 20 for free-living animals and just c. 10 years for captive-born zoo animals. Sukumar (2003) also claims that Asians have curtailed lifespans in zoos, while Lee and Moss (Chapter 2) discuss similar effects in African elephants (see also Clubb, Lee, Mar, Moss et al. subm.). Reduced reproductive success A well-documented effect of chronic stress in humans, research rodents and a host of other species is reduced fertility (see e.g., von Borell, Dobson & Prunier 2007 for an excellent overview of agricultural ungulates). In adult females, this can be manifest as impaired cycling/reduced estrus periods; premature reproductive senescence; reduced conception rates; increased pre-term fetal losses; prolonged parturitions; smaller birth weights; asymmetrical infant development; increased offspring stress responsiveness; poor maternal care (or infanticide); and/or increased infant mortality. Many of these effects stem directly from HPA axis over-activation, but additional causal factors include stress-induced prolactin elevation (Sobrinho 2003), andmore speculativelyluteolytic stress-activated protein kinases (as activated by mitogens: Yadav, Natrajan & Medhamurthy 2001). Oxytocin is also a crucial reproductive and maternal hormone, especially during parturition and in the early stages of maternal care, that can be affected by stress (see e.g., Leng, Mansfield, Bicknell, Brown et al. 1987; Pederson & Boccia 2002; Detillion et al. 2004). Of course, reduced fecundity, as with many of our previous welfare indices, is not a perfect index always indicating stress. For example, Hermes, Hildebrandt and Goritz (2004) suggest that the mere lack of breeding when young accelerates reproductive senescencealthough in zoos, such data are correlational only, so might indicate that females that failed to breed when young had sub-clinical problems only manifest overtly later in life. Furthermore, other brakes on reproduction that are independent of stress include: restricted access to males; limited mate choice; the role of nutrition (and excess weight) in many aspects of reproductive success; and dam parity and past experience (including with the infants of other females). However, these caveats acknowledged, chronic stress remains a sensible hypothesis to test when there is evidence of reproductive problems, be they low conception rates or high rates of infant death. Zoo elephants do seem to have prevalent and diverse reproductive problems: apparent low libido; poor fertility in both sexes; premature reproductive senescence in females; and, in some instances, high rates of stillbirth and infant mortality (Kurt 1995; Taylor & Poole 1998; Clubb & Mason 2002; Brown et al. 2004). For instance, Kurt (1995) reports infant mortality rates in zoo Asians as being five to six times higher than in Burmese working animals, although more recent analyses suggest the more moderate (but still unacceptable) figure of three times (Clubb, Lee, Mar, Moss et al. subm.). However, despite the work reviewed above on the non-invasive assessment of HPA activity, and also some preliminary work on African elephants to develop assays for stress-activated proteins (Bechert & Southern 2002), only one laboratory, Janine Browns, has investigated possible links between stress and reproductive success in zoo elephants. Browns work has focused on acyclicity only; it has revealed no significant links between this and HPA output (although the highest cortisol levels did seem to occur in non-cyclers), but in Africans, acyclicity was linked with elevated prolactin levels that stemmed from super-normal prolactinaemia in about one-third of the non-cycling population (Brown, Walker & Moeller 2004; Brown, Olson, Keele & Freeman 2004; Freeman, Weiss and Brown 2004). In contrast, the endocrine and behavioral correlates of reduced libido, pre- or post-natal infant mortality, reproductive senescence and the common problem of ovarian cysts, still remain unknown for zoo elephants. Furthermore, nor has any work focused on immediate maternal stress at the time of parturition, such as the effects of the management (e.g.,
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tethering, isolation) on the dams levels of oxytocin at this time. To conclude: an overview of potential welfare indices for zoo elephants A number of behavioral, physiological and health-related variables are used in scientific animal welfare assessment. The most rigorous scientific welfare research to date has typically been done on farm and laboratory animals. The best of this research uses multiple approaches, because no one single measure is perfect; it also controls for known potential confounds. Work on zoo animals, including elephants, lags very far behind. However, so far, population-level data analyses have revealed poor reproduction and reduced lifespans in both species of zoo elephants compared with protected in situ reference animals. Smaller scale studies have also recorded stereotypic behavior, and successfully assayed corticosteroid output in non-invasive ways, again for both species; additionally, one or two studies have also investigated the catecholamine output of zoo elephants, again non-invasively. However, no studies have formally compared these measures with those from protected in situ animals as a benchmark; furthermore, other potential welfare indices (e.g., those behavioral responses that field workers are expert in) have so far largely been overlooked. Does this general lack of scientific data matter? After all, for many, this type of scientific, investigatory approach to captive elephant welfare issues will seem painfully pedantic and unnecessarily labor-intensive (Isnt it obvious that small concrete enclosures are bad?). We would argue that the use of scientific welfare indices has three major advantages over just assuming that we know what elephants need for good welfare. First, when contrasting opinions exist about the potential causes of and solutions to welfare problems (cf. e.g., hypotheses about whether human contact substitutes for interactions with conspecifics, or whether environmental enrichments remove the need for large enclosure sizes), such data may eventually reveal objectively which viewpoint is correct. Second, where there are assumptions about what animals need for good welfare, based on human perspectives (e.g., they have little to do, therefore boredom must be a source of misery), such data can test them by reflecting the animals own perspectives. Third, where welfare needs are costly to meet, or in practical terms mutually exclusive (cf. e.g., having large social groups versus lots of space per animal), such data can help rank which are most important to provide. In the next section, we review what the few studies to date suggest about some potential causes of zoo elephants welfare problems. Where do elephant welfare problems come from? The five freedoms with special reference to elephants The Five Freedoms (e.g., Anonymous 1992) are tenets for ensuring good welfare, developed to facilitate the provision of adequate standards. These are as follows: (1) freedom from injury and disease; (2) freedom from hunger, thirst and malnutrition; (3) freedom from fear; (4) freedom from thermal or physical distress; and (5) freedom to express most normal behaviors. Although developed for agricultural systems, they are now incorporated into the UK zoo licensing legislation (Department of the Environment Transport and the Regions 2000). For elephants in zoos, it is the first and last items in this list that are arguably met least welland the
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last that has caused most controversy. This is because captive conditions differ enormously from the wild (Clubb & Mason 2002; Kane, Forthman & Hancocks 2005; Appendix I; Veasey 2006; Lee & Moss, Chapter 2; Poole & Granli, Chapter 1; Williams, Chapter 3)and yet we also know from other species that not all natural behaviors are essential for animal welfare (see e.g., Veasey, Waran & Young 1996a). Thus, a catalogue of great contrasts between wild and captive time budgets does not necessarily represent a list of proven causes of stress, frustration or boredom; instead, it represents a list of hypotheses that should be tested. Below we look at the evidence for the impact of three key behavioral differences between wild and captive life for elephants psychological health and welfare. What effects do curtailed freedoms to perform natural behaviors have on elephants? The differences between natural and captive life are extensive and diverse, ranging from the cognitive (Poole & Granli, Chapter 1) through to dietary and thermoregulatory challenges, the effects of which may be physical as well as psychological. However, frustration and lack of stimulation potentially caused by the curtailment of movement in zoos and unnatural social structures, have probably attracted most public criticism. Weaning age: is early removal from the dam a problem? Zoos almost ubiquitously remove calves from their mothers as infants or juvenilesa great contrast with how young elephants (especially females) live in the wild. Does this have implications for welfare? For wild African elephants in Kenya, the loss of their mother before the age of nine has lasting negative effects on female survivorship (Moss & Lee in press). However, it is near impossible to investigate whether similar effects occur in zoos because very few females are left with their mothers beyond this age. In orphanages in range countries, poorly socially integrated Asian calves apparently show more stereotypic behavior (Gara 2001)but this is not a test of weaning age per se; nor can this sad finding tell us which of these two correlated phenomena is cause, and which effect (but see Sheldrick, Chapter 16). Finally, across zoos and circuses, early-weaned Asian females reportedly had significantly lower birth rates, and were also more likely to reject or harm their own calves than other females (Kurt & Mar 1996). However, the statistical analyses in this study consisted of a series of one-independent-variable analyses with no blocking factors, and thus potential confounds were not explored (e.g., other factors correlating with being weaned early, or influential on birth rate and calf treatment). Thus overall, there is sparse, indirect evidence that premature maternal separation could have consequences beyond initial separation and therefore be a welfare issue for zoo elephants; however, no detailed studies have as yet investigated this thoroughly. Unnatural social environments for juveniles and adults: do they cause welfare problems? Differences between zoo and wild social structures include smaller group sizes (a few zoo elephants are even kept isolated), the grouping of unrelated animals, a flattened age structure (relatively few very young and very old animals in each group), a relative lack of adult males, and a lack of stability due to the movement of females between zoos for breeding (a treatment which obviously also involves transport, plus a change in enclosure, social companions and keeping staff). If zoo elephants regard their keepers as herd members, as has been claimed by some, then additional instability comes from changes in keeping staff. In wild animals, African elephants recently translocated to new reserves reportedly have
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higher fecal corticosteroid outputs than animals in longer-established parks (Millspaugh 2003). Obviously, however, translocation involves far more than just social changes, and there may also be differences between the original and the new physical environments which equally explain these effects. Wild African elephants do, however, generate more data showing that social stability per se is important. Poor maternal care of infants has been observed in herds with an abnormal social structure due to poaching (see several studies as reviewed by Bradshaw & Schore 2007). Furthermore, juvenile African elephants, especially males that are translocated at a young age to a new, elephant-free park showed behavioral problems including high aggression and the shocking killing of many rhinoceros by young bull elephants. These animals had been moved as young orphans of about eight to 10 years old, and so had matured in the absence of a social hierarchy; importing mature adult bulls to normalize the social environment rectified this problem (Slotow, van Dyk, Poole, Page et al. 2000; Bradshaw, Schore & Brown 2005; Bradshaw, Chapter 4). For zoo animals, translocation between zoos is undoubtedly a stressor, at least in the short term. Thus it was used as the biological validation for a salivary cortisol assay by Dathe et al. (1992). The hormone peaked two days after the introduction in both a newly-moved animal and the one recipient herd female that was sampled, returning to normal on the following day. Translocation between zoos was also used as the biological validation for a urinary catecholamine assay by Dehnhard (2007); moving two female elephants between zoos led to a marked temporary increase in urinary adrenaline and noradrenaline levels. Finally, one study used the transportation of a bull from the UK to a new herd in France as the biological validation for a fecal cortisol metabolite assay for Asian elephants; this animals hormone metabolite levels increased three- to four-fold, as did his levels of stereotypic behavior (Laws et al. 2007). However, further studies have shown that the magnitude of such effects varies, both between individuals and with the details of the procedure. One study, for example, showed significant urinary cortisol elevations in only one out of four Asian female elephants when mixed with unfamiliar conspecifics (Schmid, Heistermann, Ganslosser & Hodges 2001). Furthermore, in the same study, only one out of six showed a sustained increase in stereotypic behavior, with other animals apparently integrating well. Another study followed the creation of the herd at Disneys Animal Kingdom, following animals that had already been transported and habituated to the new site, but, after a period of acclimatization, were introduced to their new group members (Burks et al. 2004). During a sequential introduction, in which increases in contact from visual to tactile to full contact were allowed only gradually in a formalized procedure, smaller increases in fecal corticoids occurred than during a less structured and progressive non-sequential introduction (though it should be noted that very few animals were involved in each type of introduction, and so differences could equally have been due to the idiosyncratic temperaments and interactions involved in each instance). In this study, stress hormone levels also co-varied with submissive behavior. As for lasting and more severe effects of social upheaval, here the evidence is far patchier. Kurt (1995) reports that across European zoos, females identified as successful breeders were more likely to have matured with an adult female, and to have stayed in one stable herd all their adult life, than females who abandoned, harmed or killed calves. The latter females were more likely to have grown up with no adult female supervision, and to have been transferred between zoos multiple times (Kurt 1995). Because these two effects were confounded (and sample sizes are relatively small, and other aspects of the environment or management are not recorded), it is impossible to assess the relative effect of the abnormal juvenile environment versus the abnormal adult one. Still, this study does illustrate the potential importance of social interactions. Kurt and Mar (1996) also describe females that were moved between groups as having a lower birth rate. Just as for these
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authors apparent finding of a weaning age effect (see above), this result emerged from a series of one-independent-variable analyses with no blocking factors to control for potential confounds. However, other authors have likewise suggested that moving a cow from her social group may cause stress that impairs conception (e.g., Schmidt 1998, cited by Rees 2003). Overall, it is thus clear and unsurprising that mixing juveniles and adults with new peers, compounded with the other stressors involved in being moved between zoos, often causes transient stress. There also seems to be good evidence that for wild African elephants, dramatic humaninduced changes in social structure have negative consequences. However, there has been little or no solid research into the lasting effects (or otherwise) of chronically being in small, unrelated and/ or unstable groups in zoos, nor of being housed with non-conspecifics (i.e. Africans mixed with Asians). Furthermore, there has been no investigation of whether the absence of adult bulls affects bull calf development, nor any study of the impact of changes in keeping staff. Without such data, it is impossible to say for sure whether zoo animals simply adapt to such environments, or instead have real lasting problems which may compromise welfare. Physical restriction: does this cause welfare problems? The reduced movement of zoo elephants compared to the distances traversed in the wild, from being housed in relatively small enclosures to being chained indoors, is undeniable. Such practices may perhaps be unaesthetic, but do they necessarily cause welfare problems? Several independent studies have shown that chaining, shackling or tethering increases elephants performance of stereotypic behavior (e.g., Schmid & Zeeb 1994; Wiedenmayer & Tanner 1995; Friend 1999; Gruber, Friend, Gardner, Packard et al. 2000). Anecdotally, shackled or very physically constrained elephants are also more likely to be aggressive to humans or to their conspecifics (Kurt 1995, citing Schmid 1993), or to reject their calves after parturition (especially if also separated from their social groups; Schafternaar & Hildebrandt 2005). However, no studies seem to have looked systematically at such behavioral effects, or to have strengthened the case that chaining reduces welfare with, say, preference data, measures of physiological stress responses or assessment of the impact on oxytocin during labour. Finally, some evidence exists concerning enclosure size. This includes suggestions that enlarging enclosures reduces the performance of stereotypic behavior (Rees 2003), but the sample size in this work was just two, and of course enclosure enlargement also involves other variables (e.g., novelty), not just the provision of extra space. African elephants translocated to a new area and given a choice between a pen (625 m2) and a paddock (15,000 m2) chose the latter (Gara 1994), but, again, sample sizes were small in this study (strictly speaking, just one, if animals in a herd are considered statistically non-independent). Finally, and perhaps most convincingly of the sparse work to date, across three groups, the one in the smallest enclosure (350 m2) had fecal cortisol metabolite levels four times higher than the group in the largest 7.5 ha enclosure (Stead, Meltzer & Palme 2000). Again, the sample size here is three (taking herd as the unit of replication), and it could be that the three groups differed in stress levels for reasons quite unrelated to enclosure size. As for the previous sections, we must therefore conclude that evidence that physical restriction of freedom of movement causes poor welfare is sparse, simply because the few studies run to date have been so very small in scale. Discussion and conclusions Overall, then, what do we know (not just believe or suspect) about what elephants need
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for good psychological welfare? The short answer is: surprisingly little. Hypotheses concerning the activities and stimuli required for good welfare have not been well tested. There has been a scattering of opportunistic studies of acute responses to changes in husbandry; and the collection of population-level evidence on infant mortality, adult lifespan and stereotypic behavior (reviewed above and elsewhere by many other authors) suggests that stress-related problems are common in zoo elephants. However, no large-scale, published, epidemiological-type studies have assessed the chronic impact of different types of husbandry on reproductive success, morbidity and mortality, or stress biology. There has also been no work investigating whether stress-related changes in biology play a role in elephant morbidity and mortality; and only some work on the role of such effects in certain aspects of elephant reproductive biology (the laudable research of Brown and colleagues). There has not even been work to investigate whether controversial practices like chaining around birth cause acute stress that impairs immediate maternal care. Research is thus still very much needed, both to generate population-wide general recommendations, and to explore how welfare problems and solutions vary across individual elephants with different backgrounds and temperaments. This overall dearth of data is both surprising and depressing. It is also one reason why elephant welfare remains such a topic of controversy and of strong, diverse opinionposition statements from both sides often generating more heat than light. So, why so little real research? We suggest that three factors have held back objective work on zoo elephant welfare. The first is a lack of funding for zoo animal welfare research. Research council monies (e.g., BBSRC, NSERC, NSF), if spent on welfare at all, are monopolized by farm and laboratory animals. Furthermore, drives by zoos to raise research funds themselves are extremely rare (for one exception see below)despite the rather frequent fundraising of millions of dollars for new enclosures (whose design is thus essentially evidence-free; see e.g., Clubb, Lee, Mar, Moss et al. subm.). The second reason for the lack of substantial research on zoo elephant welfare is likely a difference in culture and resources between Europe and North America. European zoos typically have a less defensive attitude to welfare researchbut not the resources to conduct such work well. North America, in contrast, holds the worlds few full-time, respected zoo animal scientists (e.g., David Shepherdson, Nadja Wielebnowski, Kathy Carlstead and Janine Brown), but in terms of the politics of welfare, North America also has a much more polarized us and them climate (cf. Barber, Chapter 9)particularly in evidence when it comes to elephants. The third and final reason consists of logistic issues that make good science on these species challenging to conduct. Many exhibits or groups of elephants differ in numerous ways (keeper style, social grouping, whether wild-caught or captive-born, weaning age, enclosure size, mean ambient temperature, proximity of zoo visitors, etc.), and, furthermore, elephants are often moved between exhibits (Clubb & Mason 2002); it can thus be challenging to ascertain which precise aspect(s) of husbandry, past or present, cause measured effects on welfare. In addition, there is relatively little variation across zoos for some independent variables. To illustrate, few animals live in enclosures that approximate the areas they would range in the wild, and very few animals stay with their mothers much beyond infancy. Thus investigating the impact of enclosure size or weaning age is challenging: a lack of apparent effect could indicate that all zoos are equally good, or that they are actually all equally bad compared with some optimum simply unavailable for comparison. If these three factors have impeded objective welfare research on elephants to date, are they insurmountable obstacles for the future? Here, we try to look ahead more optimistically. Our review shows that several potentially useful techniques for assessing elephant welfare have been developed and validated, and simply await application. Furthermore, one major multi-zoo survey has been run in the UK over 2005-2006, by Sherwin and colleagues (Harris et al. 2006; Quaid et al. 2006),
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and was conducted with the full cooperation of and indeed financial support from the British and Irish Association of Zoos and Aquariums (BIAZA; in collaboration with DEFRA, the RSPCA and IFAW). While limited by the number and diversity of zoos in the UK and Ireland, its findings are eagerly anticipated; its methodology could provide a prototype for more ambitious work; and it reflects a refreshing level of investment by the UK zoo community. Could something similar occur in the U.S.? The international diversity of authors contributing to this volume suggests that it is not completely impossible. As for the challenges of conducting good quality research on these complex zoo populations, again, we suggest these are surmountable. Future work will need to sample sites that are both numerous and diverse to allow housing effects, both past and present, to be teased apart properly: we urge for more ambitious multi-site work that includes well-provisioned, well-protected reference to in situ populations as well as a variety of zoo and sanctuary housing, to maximize the variance in living conditions that is sampled. Such work could usefully be run collaboratively with animal welfare researchers from other fields; with epidemiologists and researchers with expertise in survivorship analyses, etc.; and, to better utilise species-typical ethological indices of state, with elephant biologists working in situ, plus elephant keeping staff. Past studbook data should be better utilized, perhaps in combination with the enclosure size data presented by the European Elephant Group in their 2002 response to Clubb and Mason 2002. Opportunistic studies at individual zoos should also continue wherever possible: although small in scale, if they each have similar outcomes, this would be informative; and, where opportunities have been missed (e.g., moves of elephants from one management system to another, or from zoos to sanctuaries), it is even possible that the effect on HPA activity could be reconstructed retrospectively from cortisol deposits laid down in hair. In the meantime, practical efforts to improve elephant housing should continuenot be placed on ice due to a lack of data. While there is something very odd about investing millions of dollars on infrastructure based on mere hunches that it will make a difference, so too is there something odd about doing nothing, save lamenting that more research is needed. Thus the lack of good welfare data does not, we should emphasize, excuse inaction. Several authors have suggested practical, useful rules of thumb to follow when upgrading facilities (e.g., Kane et al. 2005; Appendix I; Veasey 2006). Veasey (2006) suggests avenues to consider when designing facilities or management regimes for captive elephants in the absence of proper welfare data, based on elephant biology and the principles of animal welfare science. We urge that these recommendations are followed, but that all future changes in husbandry are also done with care, objectivity and humility. If elephants continue to be housed in zoos, their care must be evidence-based; their needs must be assessed and ranked; and strong claims should not be made about the welfare consequences of particular practices or changes in husbandry without firm scientific evidence. References

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Ganswindt A, Palme R, Heistermann M, Borragan S, Hodges JK. 2003. Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth. Gen Comp Endoc 134:156-166. Gara ME. 1994. The effects of boma design on stress related behaviour in juvenile translocated African elephants. Pachyderm 18:50-60. Gara M. 2001. Social behaviour of the elephants at Pinnawela elephant orphanage, Sri Lanka. Abstracts of the international elephant and rhino symposium, Vienna, Austria. p. 32-40. Gruber TM, Friend TH, Gardner JM, Packard JM, Beaver B, Bushong D. 2000. Variation in stereotypic behavior related to restraint in circus elephants. Zoo Biol 19:209-22. Harding E, Paul E, Mendl M. 2004. Animal behaviour: cognitive bias and affective state. Nature 427:312. Harris M, Harris S, Sherwin CM. 2006. Assessing the welfare, housing and husbandry of elephants in UK zoos. Proc of the Int Congress of the Int Society for Applied Ethology. p. 126. Hermes R, Hildebrandt TB, Gritz F. 2004. Reproductive problems directly attributable to long-term captivity: asymmetric reproductive aging. Anim Reprod Sci 82-83:49-60. Hunt KE, Wasser SK. 2003. Effect of long-term preservation methods on fecal glucocorticoid concentrations of grizzly bear and African elephant. Physiol Biochem Zool 76:918-928. Jones EKM, Wathes CM, Webster AJF. 2003. Strength of motivation of broiler chickens to seek fresh air after exposure to atmospheric ammonia. Br Poult Sci 44:S6-S7. Kane L, Forthman D, Hancocks D. 2005. Optimal conditions for captive elephants: a report by the Coalition for Captive Elephant Well-Being. Retrieved 2007, from http://www.elephantcare.org/protodoc_files/ new%2006/CCEWBOptimalConditionspdf.2.pdf. Kiecolt-Glaser JK, McGuire L, Robles TF, Glaser R. 2002. Emotions, morbidity, and mortality: new perspectives from psychoneuroimmunology. Annu Rev Psychol 53:83-107. Kramer B, Teixeira M, Hattingh J. 1991. The histology of the adrenal gland of the African elephant (Loxodonta africana). SA J Zool 26:193-198. Kurt F. 1995. The preservation of Asian elephants in human care: a comparison between the different keeping systems in South Asia and Europe. Anim Res & Devel 41:38-60. Kurt F, Gara M. 2001. Stereotypies in captive Asian elephantsa symptom of social isolation. Abstracts of the International Elephant and Rhino Research Symposium, Vienna, Austria. Schuling, Munster. Kurt F, Mar DK. 1996. Neonate mortality in captive Asian elephants (Elephas maximus). Z Sauget 61:155164. Laws N, Ganswindt A, Harris M, Harris S, Heistermann M, Sherwin CM. 2007. A case study: faecal corticosteroid and behaviour as indicators of welfare during relocation of an Asiatic elephant. J Appl Anim Welf Sci 10:349-358. Leng G, Mansfield S, Bicknell RJ, Brown D, Chapman C, Hollingsworth S, Ingram CD, Marsh MI, Yates JO, Dyer RG. 1987. Stress-induced disruption of parturition in the rat may be mediated by endogenous opioids. J Endocrinol 114(2):247-252. MacCaluim JM, Abeyesinghe SM, White RP, Wathes CM. 2003. A continuous-choice assessment of the domestic fowls aversion to concurrent transport stressors. Anim Welf 12:95-107. Mason G. 2007a. Stereotypic behaviour: fundamentals and applications to animal welfare and beyond. In: Mason G, Rushen J, eds. Stereotypies in captive animals (2nd ed). Wallingford, UK: CAB International. p. 325-356. Mason G. 2007b. Are wild-born animals protected from stereotypies? In: Mason G, Rushen J, eds. Stereotypies in captive animals (2nd ed.). Wallingford, UK: CAB International. p. 196. Mason GJ, Mendl M. 1993. Why is there no simple way of measuring animal welfare? Anim Welf 2:301320. Mason G, Hampton C, Wilson D, Wrbel H. 2004. Chromodacryorrhoea scores as a non-invasive means of assessing stress and disturbance in laboratory rats. Altern Lab Anim 32 (suppl 1):153-159. Mason GJ, Latham N. 2004. Cant stop, wont stop: is stereotypy a reliable animal welfare indicator? Anim Welf 13:S57-S69. 172

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Mason G, Cooper J, Clarebrough C. 2001. The welfare of fur-farmed mink. Nature 410:35-36. Mason G, Clubb R, Latham N, Vickery S. 2007. How and why should we use enrichments to tackle stereotypic behavior? Appl Anim Behav Sci 102:163-188. Masson JM, McCarthy S. 1996. When elephants weep. London, UK: Vintage. Mellor CL, Croney CC, Shepherdson D. 2007. Effects of rubberized flooring on Asian elephant behaviour in captivity. Zoo Biol 26:51-61. Millspaugh J. 2003. Use of faecal stress measures on conservation biology research: a case study of elephants in South Africa. Seminar to the Kansas State University Wildlife Society, November 14, 2003. http:// www.ksu.edu/wildlife/wildactsjoshmillspaugh.htm. Moss CJ, Lee PC. In press. Female reproductive strategies: individual life histories. In: Moss CJ, Croze H, eds. The Amboseli elephant: a long-term perspective on a long-lived species. Chicago, IL: University of Chicago Press. Pedersen CA, Boccia ML. 2002. Oxytocin links mothering received, mothering bestowed and adult stress responses. Stress 5(4):259-267. Quaid U, Harris M, Harris S, Sherwin CM. 2006. Stereotypic behaviour in captive African (Loxodonta africana) and Asian (Elephas maximus) elephants in five UK zoos. Proc of the Int Congress of the Int Society for Applied Ethology. p. 254. Rajapaksha E, Harris M, Sherwin CM, Harris S. 2006. Development and assessment of a gait scoring system for zoo elephants. Proc of the Int Congress of the Int Society for Applied Ethology. p. 56. Rees P. 2003. Asian elephants in zoos face global extinction: should zoos accept the inevitable? Oryx 37:20. Sandem AI. 2002. Eye white may indicate emotional state on a frustration-contentedness axis in dairy cows. Appl Anim Behav Sci 79:2002. Schafternaar W, Hildebrandt TB. 2005. Veterinary guidelines for reproduction-related management in captive female elephants. Elephant Taxon Advisory Group, European Association of Zoos and Aquaria. EAZA, Amsterdam, the Netherlands. Schmid J, Heistermann M, Ganslosser U, Hodges JK. 2001. Introduction of foreign female Asian elephants (Elephas maximus) into an existing group: behavioural reactions and changes in cortisol levels. Anim Welf 10:357-372. Slotow R. 2002. Stressed elephant dung, brucellosis in buffalo and lions. Interview on Earthbeat. Broadcast on October 26, 2002. http://www.abc.net.au/rn/science/earth/stories/s707995.htm. Slotow R, van Dyk G, Poole J, Page B, Klocke A. 2000. Older bull elephants control young males. Nature 408:425-426. Sobrinho LG. 2003. Prolactin, psychological stress and environment in humans: adaptation and maladaptation. Pituitary 6:35-39. Stead SK, Meltzer DGA, Palme R. 2000. The measurement of glucocorticoid concentrations in the serum and faeces of captive African elephants (Loxodonta africana) after ACTH stimulation. J S Afr Vet Assoc 71:192-196. Sukumar R. 2003. The living elephants: evolutionary ecology, behaviour, and conservation. Oxford, UK: Oxford University Press. Szdzuy K, Dehnard M, Strauss G, Eulenberger K, Hofer H. 2006. Behavioural and endocrinological parameters of female African and Asian elephants Loxodonta africana and Elephas maximus in the peripartal period. Int Zoo Yearb 40:41-50. Taylor VJ, Poole TB. 1998. Captive breeding and infant mortality in Asian elephants: a comparison between twenty western zoos and three eastern elephant centers. Zoo Biol 17:311-332. Terio KA, Marker L, Munson L. 2004. Evidence for chronic stress in captive but not free-ranging cheetahs (Acinonyx jubatus) based on adrenal morphology and function. J Wildl Dis 40:259-266. Toates F. 1997. Stress: conceptual and biological aspects. New York, NY: John Wiley & Sons. Touma C, Palme R. 2005. Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann NY Acad Sci 1046:54-74. 173

Veasey JS, Waran NK, Young RJ. 1996a. On comparing the behaviour of zoo housed animals with wild conspecifics as a welfare indicator. Anim Welf 5:13-24. Veasey JS, Waran NK, Young RJ. 1996b. On comparing the behaviour of zoo housed animals with wild conspecifics as a welfare indicator using the giraffe as a model. Anim Welf 5:139-153. Veasey J. 2006. Concepts in the care and welfare of captive elephants. Int Zoo Yearb 40:63-79. von Borell E, Dobson H, Prunier A. 2007. Stress, behaviour and reproductive performance in female cattle and pigs. Horm Behav 52:130-138. Wall J, Douglas-Hamilton I, Vollrath F. 2006. Elephants avoid costly mountaineering. Curr Biol 16:527529. Warburton H, Mason G. 2003. Is out of sight, out of mind? The effects of resource cues on motivation in the mink (Mustela vison). Anim Behav 65:755-762. Wasser SK, Hunt KE, Brown JL, Cooper K, Crockett CM, Bechert U, Millspaugh JJ, Larson S, Monfort SL. 2000. A generalized fecal glucocorticoid assay for use in a diverse array of non-domestic mammalian and avian species. Gen Comp Endoc 120:260-275. Weary DM, Braithwaite LA, Fraser D. 1998. Vocal response to pain in piglets. J App Anim Behav Sci 56:161-172. Weibull AC, Eriksson H. 1998. Short-term gland secretion in the African elephant: tourist disturbance or social interactions as source for secretion? Afri J Ecol 36:360-367. Wiedenmayer C, Tanner R. 1995. Untethered housing of Asian elephants (Elephas maximus) at Zurich Zoo. Int Zoo Yb 34:200-205. Yadav VK, Natrajan T, Medhamurthy R. 2001. Increased stress-activated protein kinase activity during PGF2alphas-mediated apoptotic cell death in buffalo corpus luteum. Proc XXV All India cell biol conf, Bangalore, India. p. A59.

Professor Georgia Mason is Canada Research Chair in Animal Welfare at the University of Guelph, and Visiting Professor in Animal Welfare Physiology at the Royal Veterinary College (London). She obtained her undergraduate degree in zoology and Ph.D. in animal behavior from Cambridge University, before taking up a Clare College Junior Research Fellowship. She then held a demonstratorship (assistant professorship) in Vertebrate Biology at Oxford Universitys Zoology Department, followed by a BBSRC David Phillips Research Fellowship. She moved to Canada in 2004. Her research interests focus on animal welfare: its objective assessment, and how early experience and species differences protect or predispose animals to problems. She has c. 100 publications, including a report on elephant welfare in European zoos: see http://www.uoguelph.ca/abw/gmason/. She may be contacted at: Animal Sciences, University of Guelph, Ontario, Canada N1G 2W or at gmason@uoguelph.ca. Jake Veasey is the Head of the Department of Animal Management and Conservation at Woburn Safari Park. He studied at the universities of London, Edinburgh and Glasgow, gaining degrees in zoology, applied animal behavior and animal welfare, and a Ph.D. in behavioral ecology respectively. Jake has worked alongside elephants in Zimbabwe, Kenya, Swaziland and South Africa, and is currently responsible for the management of a group of Asian elephants within Woburn Safari Park. He has championed the development of management guidelines for elephants within the UK and beyond in which elephant welfare is fundamental, and management is subsequently based around the biology of the species as well as the needs of the individuals. He may be contacted at Woburn Safari Park, Woburn, Bedfordshire MK17 9QN, United Kingdom or at jake.veasey@woburnsafari.co.uk.
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Debra L. Forthman The two chapters in the section that follows illustrate well what can be accomplished when science is applied to the many tasks related to the well-being of elephants in captivity. In the first chapter, Kinzley describes a program at the Oakland Zoo that would have made Hediger proud. Based on knowledge of the species natural history, it promotes behaviors more similar to those of wild elephants. The zoos elephant managers went far beyond the simple provision of toys or the use of free contact training sessionsor even the treat of spatially and temporally clumped browse that the elephants consume in short order. Instead, Kinzley and her staff decided to get their elephants moving, at least for the minimum distances documented among wild elephants. She describes how this is accomplished, even in an urban zoo with limited space: largely by dint of extraordinary effort and dedication on the part of her staff. Whittaker and Laule address a different system, but one also grounded firmly in scientific principles, in this case those of learning. They describe the development, application and advantages of Protected Contact (PC), an elegant integration of operant and classical conditioning procedures based entirely on positive reinforcement (rewards) and negative punishment (time-outs). The PC system developed by Desmond and Laule adapts techniques they both used in earlier work with large marine mammals. It is designed to ensure the safety of both elephants and staff, while eliminating entirely the use of negative reinforcement and physical punishment in the elephants daily lives. Kinzleys program offers elephants in captivity the ability to engage in fundamental aspects of their behavioral ecologyforaging and travel. Whittakers and Laules system provides elephants with cognitive stimulation that involves a degree of autonomy and choice. Both illustrate that it is possible to give back, even in limiting environments, certain key aspects of elephants lives in the wild.

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Colleen Kinzley Oakland Zoo Applied behavioral research has served as an effective management tool for many species of captive animals. Bridging the gap between research-based principles of animal behavior and animal management has resulted in improved welfare for numerous companion animals, livestock and zoo animals (Grandin 2001). For captive wildlife, changes in management, social structure and environment that allow animals to engage in behavior more closely resembling that of their counterparts in the wild have been shown to improve welfare (Lukas 1999; Shepherdson, Carlstead & Wielebnowski 2003). Decades of elephant field research have provided a wealth of information on the behavior and activity budgets of elephants in the wild (Wyatt & Eltringham 1974; Douglas-Hamilton & Douglas-Hamilton 1975; Hanks 1979; Eltringham 1982; Moss 1988). Studies have shown that elephants are active much of the day and night and travel great distances. They are also socially and behaviorally complex animals as demonstrated in behaviors like aunting of calves and tool use (Douglas-Hamilton & Douglas-Hamilton 1975; Moss 1988). This knowledge of species-typical behaviors and activity budgets can serve as a welfare model for captive elephants. At the Oakland Zoo, applied behavioral research has been used to guide management and facility changes with the goal of increasing species-typical behavior and activity budgets and decreasing stereotypic behavior. Using behavioral measures of elephants in the wild, behavioral goals were established for the four African elephants (one bull, three cows) at the Oakland Zoo. During observation periods, many behaviors were recorded and assessed; however, foraging and feeding time, distance traveled and the incidence of abnormal stereotypic behavior were used to measure welfare (Laule 1993). Initially, our observations took the form of ad libitum sampling or field notes (Martin and Bateson 1987). Large amounts of descriptive information about the activities, interactions and locations of the elephants were recorded. Keepers and volunteers comprised the observation team; each member weekly compiled a couple hours of observation notes. The team would meet regularly to discuss the observations and possible management changes in shifting, enrichment and feeding, for example. This early work set the stage for what would become a management system that relied on feedback in the form of behavioral data. A formal data collection system was implemented that used scan sampling at five-minute intervals along with ad libitum sampling for all rare and social behaviors (Martin and Bateson 1987). In the wild, approximately four hours of an elephants day are spent in rest and the remainder spent in activities like foraging, dusting, bathing, traveling and socializing (Eisenberg 1981; Moss 1988). Based on these behavioral measurements, a management change was made that allowed the Oakland Zoo elephants to stay outside at night during the eight months of mild weather.
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This change resulted in increased overall physical activity, increased species-typical behaviors and near elimination of stereotypic swaying between the hours of 4:30 p.m. and 7:00 a.m. Stereotypic swaying in one female was reduced from an average of five hours per night to 30 minutes and in another the behavior was eliminated entirely during the nighttime hours. Stereotypic swaying is not observed in elephants in the wild and in captivity it is observed only in those elephants that have spent long periods of time (typically overnight, and an average of 16 hours per day) on front and rear leg chains that severely limit their movements to a few feet in any direction (Galloway 1991; Schmid 1995). Specific motivational factors, like feeding motivation and frustrated physical activity, have been linked to the development and performance of stereotyped behaviors in intensely confined animals (Lukus 1999). The high level of physical activity in elephants, the absence of stereotypic swaying in elephants that havent experienced persistent long-term chaining and the decrease in stereotypic swaying with the opportunity for increased activity suggest frustrated physical activity as a possible motivational factor in stereotypic swaying. The frequent lack of extended feeding opportunities could also be contributing to the development of stereotypies in elephants through frustrated feeding motivation. In the wild, elephants spend 16-18 hours per day foraging and feeding (Eisenberg 1981; Moss 1988; Estes 1999). The Oakland Zoo elephants were spending an average of eight hours per day in feeding and foraging behaviors with half of that time occurring during the keepers eighthour work day. To increase feeding and foraging during the 16 hours that keepers were not present, the evening diet was divided into multiple feedings to be fed by the night keeper at 8:00 p.m., 11:00 p.m., 3:00 a.m., and 6:00 a.m. Follow-up observations revealed that foraging and feeding time increased on average 3.5 hours. The 3:00 a.m. feeding was eliminated because it frequently woke the elephants, and the 6:00 a.m. was moved to 5:00 a.m. because they were typically awake and active by that hour. Browse constitutes up to 70 percent of the diet of elephants in the wild (Field and Ross 1976; Sukumar 1989). For captive elephants, the manipulations involved in consuming browse extend feeding time without increasing caloric intake. Observations of the Oakland Zoo elephants demonstrated a positive correlation between increased browse and increased feeding time. Currently the minimum amount of browse provided is 100 lbs of browse per elephant per day with the goal of providing free choice browse. The natural packaging provided by browse food items inspired changes in feeding strategies aimed at increasing the time spent feeding on hay and supplemental food items. Devices including plastic barrels of varying sizes, elevated feeders and heavy PVC tubing are used to create foraging challenges and extend feeding time. The distances traveled by elephants in the wild over a 24-hour period vary greatly but figures available on the lower end of the spectrum range from seven to 13 miles per day (Sukumar 2003). By dividing the elephants outdoor space into measured blocks, a conservative measurement of distance traveled can be calculated by adding the distance between center points each time an elephant moves from one block to the next. Initially, the elephants traveled an average one-half mile per day. The period during which they traveled the greatest distance was in the morning when the elephants were first shifted into the exhibit. The morning diet and enrichment were spread and hidden throughout the exhibit which motivated them to walk back and forth, first seeking out favorite items, then coming back to things that were passed up earlier. To increase distance traveled, spread feedings replaced the other four stationary daytime feedings, resulting in five spread feedings per day. This change in feeding strategies increased distance traveled to an average of two miles per day. The Oakland Zoo expanded its outdoor elephant space from approximately 1.25 acres to
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approximately six acres. This change has resulted in many qualitative improvements that have provided a much more complex habitat for the elephants. The expanded space allows the elephants to choose between full sun and deep shade, and whether they want to be visible to zoo guests or each other or both. The majority of the expanded space is also irrigated pasture. Where previously less than two percent of their time was spent grazing on the grass that grew on the edges of their dirt exhibit, they now spend up to 23 percent of their time grazing. The increased space and habitat complexity has also resulted in a 51 percent increase in distance traveled. Applied behavioral research has been used with the Oakland Zoo elephants to successfully implement management and facility changes, resulting in increased species-typical behaviors and activity budgets. Maximizing the time the elephants spend outside, providing their diet across all of their hours of activity, and presenting and feeding a diet that encourages the elephants to either travel or work for food have been successful management strategies. Facility expansion provided increased space and environmental complexity, resulting in increased species-typical behavior and distance traveled while providing the elephants with greater choice and control over their environment. References

Douglas-Hamilton I, Douglas-Hamilton O. 1975. Among the elephants. London, UK: Collins. Eltringham SK. 1982. Elephants. Dorset, UK: Blanford Press. Field CR, Ross IC. 1976. The savanna ecology of Kidepo Valley National Park. II. Feeding ecology of elephant and giraffe. E Afr Wildl J 14:1-15. Galloway M. 1991. Update on 1990 chaining survey. Paper presented at the 12th Elephant managers workshop. Syracuse, NY. Grandin T. 2001. Transferring results of behavioral research to industry to improve animal welfare on the farm, ranch, and the slaughter plant. D.G.M. Wood-Gush memorial lecture. 35th International congress of the society of applied ethology, Davis, CA. Hanks J. 1979. The struggle for survival: the elephant problem. New York, NY: Mayflower Books. Laule G. 1993. The use of behavioral techniques to reduce or eliminate abnormal behavior. Anim Welf Ctr News 4(4):1-11. Lukas KE. 1999. A review of nutritional and motivational factors contributing to the performance of regurgitation and reingestion in captive lowland gorillas (Gorilla gorilla gorilla). Appl Anim Behav Sci 63:237-249. Martin P, Bateson P. 1987. Measuring behavior: an introductory guide. Cambridge, UK: Cambridge University Press. Moss CJ. 1998. Elephant memories: thirteen years in the life of an elephant family. New York, NY: William Morrow. Schmid J. 1995. Keeping circus elephants temporarily in paddocks: the effects on their behavior. Anim Welf 4:87-101. Shepherdson DJ, Carlstead KC, Wielebnowski NC. 2003. Cross-institutional assessment of stress responses in zoo animals using longitudinal monitoring of faecal corticoids and behavior. Final proof, UFAW. Sukumar R. 1989. Ecology of the Asian elephant in Southern India. II. Feeding habits and crop raiding patterns. J Trop Ecol 5:384-396. Wyatt JR, Eltringham SK. 1974. The daily activity of the elephant in the Rwensori National Park, Uganda. E Afr Wildl J 12:273-289.

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Colleen Kinzley is the General Curator of the Oakland Zoo. She has been caring for captive elephants since 1983. Colleen initiated and maintains applied behavioral research on one male and three female captive African elephants. She participates in field research on African elephants in Namibia that examines the social behavior of bull elephant society. Through operant conditioning training, she has trained a captive elephant to participate in forced choice testing to determine seismic detection levels. Colleen also has participated in other research projects, including evaluation of temporal gland secretions, monitoring testosterone in an adult bull and testing efficacy of ibuprofen and phenylbutazone medications in elephants. She implemented a Protected Contact Training and Management program for one male and three female African elephants in 1991, hand-raised an African elephant bull calf and expressed milk from an African elephant cow for ongoing analysis of milk. Colleen coordinates fundraisers and events to provide financial support to and recognition of several elephant research and conservation projects, including over $180,000 to date raised for the Amboseli Elephant Research Project. Colleen may be contacted at Oakland Zoo, P.O. Box 5238, 9777 Golf Links Rd., Oakland, CA 94605 or at colleen@oaklandzoo.org.

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Margaret Whittaker1 and Gail Laule1,2 Active Environments1 and Wildlife in Need2 Captive elephant management in the 21st century: by all appearances it is as emotionally charged and contentious as it was in previous decades. Elephants continue to be the subject of unprecedented attention, scrutiny and debate. Numerous guidelines, standards and recommendations for all aspects of elephant care including housing, space, social groupings and training have been produced, with varying degrees of objective scientific evaluation (Clubb & Mason 2002; AZA 2003; Olson 2004; CCEW 2005; Kane, Forthman & Hancocks, Appendix I; Kane, Forthman & Hancocks, eds., Appendix II). Consensus on management issues has been hampered by a lack of concise and candid information about each management system and the specific tools and techniques used and approved within it (AZA 2001; Olson 2004). Furthermore, both of the primary management systems, traditional free contact and the more recent protected contact, seem to be connected to distinctly different perspectives on how elephants are viewed, and managed, relative to other captive species. The free contact approach is most closely aligned with the view that elephants have social, psychological and physical needs that are so distinct and unique from any other species that they require a whole set of specialized management techniques. Although this may appear reasonably sound on the surface, this view has led to the use of certain methods of management that are counter to conventions used with most other taxa. For example, keepers would never routinely enter the same space with a bear or rhino, yet it is done with elephants. It would be considered unacceptable for a keeper to strive for social dominance over a snow leopard, yet free contact keepers attempt to establish and maintain this type of relationship over elephants. It would be unacceptable to routinely employ the techniques of negative reinforcement and physical punishment with gorillas, yet these techniques are used regularly with elephants in a free contact system. In contrast, protected contact is most closely aligned with the perspective that elephants are no more or less unique than any other species held in captivity. This view acknowledges that elephants are indeed unique, with their own specific needs, yet insures that management techniques are consistent with the rules and practices applied to other captive animals. It also encourages the free flow of information, for there is much that can and should be learned and applied across species. There are options in management systems and each should be carefully evaluated on the basis of its relative costs and benefits for elephant care and welfare. Acknowledging the highly opinionated and contentious environment surrounding elephant management issues, we suggest three basic rules to follow to aid this evaluation and to maximize the potential welfare benefits for captive elephants. First, strive for utmost clarity in defining and implementing the system being used. Second, when making choices in methods, tools and techniques, always choose the most positive
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option, and be prepared to defend and support your choice. Third, in the decision-making process, use science when it is available and fairness and reason when it is not. Move past differences in opinion and into the realm of fact and objective assessment whenever possible. To do so completes the loop, as objective assessment leads to, and requires, clarity. Clarity in defining protected contact A system of managing any captive animal has several key elements: it is definableall the tools, techniques and underlying tenets can be clearly defined, described and applied to a variety of situations and contexts. It provides for all aspects of the animals care and is transferable among staff members and to other institutions if the animal is relocated. Protected contact and free contact are both systems for managing elephants that meet all the criteria described above. The official American Zoo and Aquarium Association (AZA) definition of protected contact is as follows (2003): Handling of an elephant when the keeper and the elephant do not share the same unrestricted space. Typically, in this system, the keeper has contact with the elephant through a protective barrier of some type, while the elephant is not spatially confined and may leave the work area at will. This is contrasted with the definition of free contact where the keeper and elephant do share the same unrestricted space. The two primary elements in these definitions are the physical location of elephant and keeper, and the presence or absence of a physical barrier. There is no reference to the tools, techniques or human/animal social dynamics (important elements of each system) that distinguish one form of management from the other. Protected contact has two equally important fundamental objectiveskeeper safety and animal welfare (Desmond & Laule 1991, 1993; Lenhardt 1991). As the original creators and architects of protected contact, and for purposes of clarity, we define protected contact in the following way: protected contact is a system for managing elephants that uses positive reinforcement training as the primary method to modify behavior and gain the voluntary cooperation of the animal. Physical punishment is prohibited. Directing the positioning and movement of the elephant and shaping behavior is achieved through the use of targets. Keeper safety is achieved by elephant and keeper positioning relative to each other and to a barrier, which typically separates human and animal spaces. Trainers function outside the elephant social hierarchy and do not attempt to establish a position of social dominance (Laule & Whittaker 2000). Since the introduction of protected contact to the zoological community in 1991, over half the zoos in the United States have converted their programs to this management system. However, during this time there has been significant drift in many facilities in how protected contact is implemented. For example, in our travels around the country we encounter elephant management practices that are called protected contact or modified protected contact, in which trainers simply move to the other side of the physical barrier and give commands to the elephants. In these situations, the trainer may continue to carry the ankus, use an authoritative voice to give commands and maintain a dominance-based relationship. According to the AZA definition, this would qualify as protected contact. According to our definition, it does not. Protected contact is not free contact conducted from the other side of a barrier. It is a separate and distinct form of elephant management that is defined by its specific tools and techniques, not just by keeper position and the presence of a barrier. The simplistic view allows, and even invites, misinterpretation. These various modifications of protected contact have been fueled and supported by AZA in two ways. The Elephant Husbandry Resource Guide published in 2004 is the husbandry manual distributed by the AZA Elephant Taxon Advisory Group (TAG) to all member institutions housing elephants. The Principles of Elephant Management (PEM) course is required for all elephant
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managers of AZA-accredited facilities. Both the Resource Guide and the PEM course promote the position that there are no distinct differences between free contact and protected contact training systems, only a continuum of options. Although used routinely throughout the industry and in publications, journals and conference proceedings, the terms free contact and protected contact never appear in the entire Resource Guide and are mentioned cursorily in the PEM course. Unfortunately, this position inhibits rather than assists elephant managers in evaluating the relative costs and benefits of the choices they make and the impact of those choices on animal welfare (Adler 1996; Laule & Whittaker 2000). Clear and concise thinking is fundamental to any problem-solving processwe must strive for clarity to assess and choose our options. Although there are certainly similarities between systems, it is the differences that may be most relevant, and we have to be willing to look at these openly and honestly in order to assess options and make an informed choice. Tools of protected contact The tools of protected contact are simple: a conditioned reinforcer such as a whistle or clicker, targets of varying lengths and food reinforcers. The primary technique and foundation of protected contact training is positive reinforcement. Operationally, we are gaining the elephants voluntary cooperation in everything from basic movement and daily husbandry routines to more invasive medical procedures. To do so requires addressing proactively any signs of fear and discomfort in relation to a particular event, person, situation, location or object (Laule 2003). This is done through desensitization, a powerful and versatile training technique that is integral to protected contact. Desensitization works by pairing positive reinforcement with the frightening event or object. Through the direct relationship between the fear-inducing stimulus and the presentation of many positive reinforcers, over time fear associated with that event is diminished. According to the AZA PEM course notebook, the official tool list for protected contact includes the ankus or guide as it is now referred to euphemistically, the premise being that the tools of free and protected contact are interchangeable. In fact, the use of an ankus in protected contact violates the fundamental principles of a system based on positive reinforcement, and subsequently diminishes its welfare benefits to elephants (Laule et al. 2000). This position also inhibits clear, informed decision-making when assessing, choosing and transferring a management system. The role and context of the human/animal relationship is also an important element of elephant management systems. In protected contact, it is not necessary, nor is it appropriate, for the trainer to be socially dominant. In fact, attempts should be made to diminish this type of relationship. This is in direct contrast to traditional free contact training in which the establishment, and maintenance, of human social dominance over the elephants is fundamental. Positive reinforcement is the primary method of behavioral modification in a true protected contact system. This means that all positive reinforcement options are pursued and exhausted before resorting to any unpleasant or aversive techniques. We recognize that in the real world there will be those times when negative reinforcement or non-physical punishment may be necessary. We acknowledge that all elements of operant conditioning contribute to learning. However, being true to a protected contact management system requires that the highest priority of implementation is the strict commitment to use positive reinforcement as the primary means by which new behavior is taught, undesirable behavior is addressed and non-routine procedures are dealt with. Finally, protected contact is designed to allow elephants to exercise a high degree of choice and control, to experiment and to make mistakes without negative consequences. When undesirable behavior, such as non-compliance or aggression, must be addressed, operant conditioning offers
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three appropriate and acceptable methods to use: extinction, training of incompatible behaviors and mild, non-physical punishment. The only form of punishment that has a place in protected contact is the use of the time-out, which briefly removes the animals opportunity to earn positive reinforcement of any kind. Physical punishment is prohibited and the only exception is a lifethreatening situation for person or animal. Choosing the most positive option We have choices in what we do and how we do it. This rule is simpleassess the options objectively and deliberately choose the most positive one. For example, finding the most positive training approach applies across species and to all situations. In dog training, we can choose positive reinforcement methods over negative reinforcement and punishment; verbal correction over physical correction; a cooperative relationship over a dominance-based one; and so on (Donaldson 1996; McConnell 2003). For progressive dog trainers, the more positive the method, the more preferred it is. In horse training, individuals like Tom Dorrance (1987) and Pat Parelli (2003) have made careers, and improved the welfare of countless horses, by advocating the most positive methods of training. In the biomedical community, Institutional Animal Care and Use Committees are directed to evaluate studies based on this principle. The Animal Behavior Societys guidelines (2000) on the use of Aversive Stimulation and Deprivation with animals in behavioral research state: To minimize possible suffering of the animal, the investigator should ascertain that there is no alternative way of motivating the animal, and that the levels of deprivation or aversive stimulation used are no higher than necessary to achieve the goals of the experiment. Alternatives to deprivation include the use of highly preferred foods and other rewards which may motivate even satiated animals. (p. 4) In the keynote speech at an Ethics and Animal Welfare conference in 1998, James Battye of the Department of Philosophy at Massey University in New Zealand made the following comments regarding the treatment of animals in biomedical research: If people who work with animals are seen to have fair and reasonable views, are seen to be putting them into practice and to be working on lifting their game still further, public confidence and respect will surely follow. If you can show that not only does the good you do outweigh the bad, but also that it does so to the greatest possible extent, and that you are always on the lookout for new ways to increase that margin, you can open the doors of your laboratories with pride. Generally speaking, most zoo professionals are already applying this philosophy to captive animals in several ways. Zoo-wide training using positive reinforcement and avoiding negative reinforcement is becoming commonplace in the United States (Reichard 1992; Whittaker 2006). The move to husbandry training is a very real way of improving animal care and welfare by gaining the animals voluntary cooperation in veterinary procedures while directly reducing the accompanying fear and anxiety (Reinhardt, Cowley, Scheffler, Vertein et al. 1990; Videan, Fritz, Murphy, Borman et al. 2005). This approach is preferable to restraining, coercing, tricking or forcibly administering necessary medical care (Laule & Whittaker 1998). For example, presenting a leg for an injection is a far more positive option than being chased and darted (Lambeth, Hau,Perlman et al. 2006). With elephants, we can apply this criterion to actively seek the most positive management
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system to use. For example, maximizing the use of positive reinforcement and minimizing the use of negative reinforcement in all aspects of care and training is the first step (Abadie 1997). Second, assess the possible tools and make the most positive choice. For example, evaluating the choice between the use of an ankus or a target, would look like this: An ankus: is used to cue and shape behavior must be established as an aversive stimulus and functions as a negative reinforcer is traditionally used to maintain the trainer in a socially dominant position is used to mete out physical punishment A target: is used to cue and shape behavior is a neutral object the animal learns to move towards is associated exclusively with positive reinforcement If we assume that either tool is sufficient to train new behaviors and maintain existing ones, clearly using a target is the most positive method. In our experience, we have never encountered a behavior we cannot cue and shape using a verbal command or hand signal and a target. Furthermore, no matter how gently the ankus may be used with an animal, at some point it had to be established as a negative reinforcer in order to be effective: that means causing enough pain and discomfort that the animal remembers, and seeks to avoid that experience by complying. It seems reasonable to ask, why would we want to continue to use a tool that is unnecessary and carries with it a history of pain, discomfort and human dominance? Doesnt that clearly break the rule of always choosing the most positive option? Science-based decision-making Science-based is a term being used a lot these days, often more as a wish than a reality, primarily because there are huge gaps in our knowledge of what elephants need and what methods best meet those needs. Therefore, a concerted effort is required to gather credible information from all areas of elephant experience, as well as objective information on other species that is relevant and appropriate to extrapolate in order to make sound decisions that maximize animal welfare. What does science say about our choices in training strategies? Even a cursory search of the literature will reveal overwhelming evidence that the use of aversive techniques, particularly physical punishment, has many associated risks and negative consequences (Hediger 1950; Chance 1994; Hemsworth & Coleman 1998; Pryor 1999). Whether studying its use with children (referred to as power assertion) or in training dogs (Donaldson 1996), or in insuring compliance in behavioral studies with primates (Reinhardt 1992; Laule 2003), aversive techniques have been repeatedly found to be related to aggression, an increase in undesirable behaviors and the potential for suffering and diminished welfare (Moseley & Davis 1989; Reinhardt et al. 1990; Reinhardt 1992; Broom & Johnson 1993). Fairness and reason would lead us to a similar conclusion. Studies with farm animals have shown that high levels of fear responses are associated with negative handling methods. This is somewhat surprising as these are domesticated species. In one study on handling of heifers using negative methods including hits, slaps and kicks, remote blood sampling through indwelling jugular catheters showed both acute and chronic stress response in fearful animals (Breuer, Coleman & Hemsworth 1998). A study on dog training methods found that dogs trained exclusively using reward-based
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methods were reported to be significantly more obedient than those trained using either punishment or a combination of reward and punishment. Dogs trained using punishment also exhibited more problematic behaviors including chewing household objects, stealing food and over-excitement (Hiby, Rooney & Bradshaw 2004). Some studies also warn that just because animals comply and appear to be comfortable does not mean that is so. Markowitz and his colleagues (Line, Clarke & Markowitz 1987; Line, Morgan, Markowitz & Strong 1989) as reported by Forthman and Ogden (1992) have cautioned animal managers never to presume, without supporting data, that animals have become habituated to routine procedures and handling because their studies have demonstrated prolonged alterations in heart rate and cortisol levels after such routine procedures as cage cleaning. Field researchers, who often have experience with vast numbers of animals over extended time periods, have developed information that is important to consider. Poole (2001) reports that, from her experience, African elephants do not discipline their young, nor is discipline natural in elephant society [and] therefore something that an elephant can understand. Poole states that calves are protected, comforted, cooed over, reassured, and rescued, yes, but punished, no. These are just a few examples of the science that is available and worthy of review in making decisions about how we manage elephants to maximize their welfare. If we accept the premise that elephants share an array of basic needs with other captive species, then a wealth of information and experience with a wide array of species is available, some of which can logically be extrapolated to decisions about elephant welfare. Yet with huge gaps in our knowledge and in the absence of science to guide our decisionmaking, we must have another mechanism to assess options and make informed choices. As Albert Einstein said, All things thatmatter cannot be counted and many things that can be counted dont matter. In the absence of science, Battye (1994) suggests that fairness and reason are concepts upon which important decisions regarding animal welfare, and our ethics about it, can be grounded. By way of illustration, he rewrites the golden rule to read: Treat others as you would want to be treated if you had their needs and interests, not as if you were in their place with your own needs and interests. His closing words to the biomedical community are relevant to the captive elephant community as well: If you are determined to be fair and reasonable, there is nothing to fear. We agree, and suggest that, where science leaves off, we must be willing to support and defend our subjective decisions based on the principles of fairness and reason. Conclusions There is a great deal of discussion these days about the importance of giving back choice and control to captive animals, and the huge benefits gained in the process. It is important to recognize that we humans do have tremendous choice in how and what we do. And, ultimately, we are the ones with the greatest control. So, the purpose of this paper is to suggest ways we can use our choices and control to better the lives of the elephants we care for. It is our belief that we can maximize the welfare of captive elephants by recognizing their uniqueness, as well as their similarities with other species. So the three rules we suggest are simple and reasonable, and can be applied to all captive animals: First, be clear and concise in what you do, and why youre doing it; second, when making choices about how to manage and care for elephants, always select the most positive option. And finally, in making your choices, use science when it is available, and fairness and reason when its not.
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Abadie M. 1997. Medical management of an Asian elephant herd in a protected contact system. Paper presented at the AZA ann conf, Minneapolis, Minnesota, September. Adler JJ. 1996. Hands-off, protected contact or free contact: linguistic and other problems in elephant husbandry. Intl Zoo News 43(1):18-24. American Zoo and Aquarium Association Regents. 2001. AZA schools for zoo and aquarium personnel: principles of elephant management. Silver Spring, MD: AZA. American Zoo and Aquarium Association. 2003. Standards for elephant management and care. Silver Spring, MD: AZA. Animal Behavior Society. 2000. Guidelines for the treatment of animals in behavioral research and teaching. Handbook of the executive committee, committee chairs, liaisons, and representatives. Section 27(d.3). Bloomington, IN: Animal Behavior Society. Battye J. 1994. Ethics and animal welfarewhere do we go from here? Proc conf on Animal welfare in the twenty-first century: ethical, educational, and scientific challenges conf, Christchurch, New Zealand, April. p. 3-10. Broom DM, Johnson KG. 1993. Stress and animal welfare. London, UK: Chapman and Hall. Breuer K, Coleman GJ, Hemsworth PH. 1998. The effect of handling on the stress physiology and behaviour ofnonlactating heifers. Proc 29th ann conf Australian Soc Study Anim Behav. p. 8-9. Chance P. 1994. Learning and behavior, 3rd ed. Pacific Grove, CA: Brooks/Cole Publishing Company. Clubb R, Mason G. 2002. A review of the welfare of zoo elephants in Europe. Horsham, UK: RSPCA. Desmond T, Laule G. 1991. Protected contact elephant training. Proc AAZPA ann conf. p. 606-613. Desmond T, Laule G. 1993. The politics of protected contact. Proc AZA ann conf. p. 12-18. Donaldson J. 1996. The culture clash. Berkeley, CA: James and Kenneth Publishers. Dorrance T. 1987. True unity: willing communication between horse and human. Tuscarora, NV: Give-ita-Go Enterprises, Word Dancer Press. Elephant Managers Association. 1999. The EMA standard guidelines for elephant management. JEMA 10:203-204. Forthman D, Ogden J. 1992. The role of behavior analytic principles in zoo management: today and tomorrow. J Appl Behav Anal 25:647-652. Hediger H. 1950. Wild animals in captivity. London, UK: Butterworth. Hemsworth PH, Coleman GJ. 1998. Human-livestock interactions: the stockperson and the productivity and welfare of intensively-farmed animals. Wallingford, UK: CAB International. Hiby EF, Rooney NJ, Bradshaw JW. 2004. Dog training methods: their use, effectiveness and interaction with behaviour and welfare. Anim Welf 13:63-59. LambethS, Hau J,Perlman J, Martino M, Schapiro S.2006.Positive reinforcement training affects hematologic and serum chemistry values in captive chimpanzees (Pan troglodytes). AJP 68(3):245256. Laule G. 2003. The use of positive reinforcement training techniques to enhance the care, management, and welfare of primates in the laboratory. JAAWS 6(3):163-174. Laule G, Whittaker M. 1998. The use of positive reinforcement techniques in the medical management of captive animals. Proc joint conf AAZV & AAWV. p. 383-387. Laule G, Whittaker M. 2000. Protected contact: beyond the barrier. Paper presented at the AZA Ann Conf, Orlando, FL, September. Lenhardt J. 1991. Elephant handling: a problem of risk management and resource allocation. Proc AAZPA. p. 569-575. Line S, Clarke AD, Markowitz H. 1987. Plasma cortisol of female rhesus monkeys in response to acute restraint. Lab Prim News 26:1-4.

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Line S, Morgan KN, Markowitz H, Strong S. 1989. Heart rate and activity of rhesus monkeys in response to routine events. Lab Prim News 28:9-12. McConnell PB. 2003. The other end of the leash: why we do what we do around dogs. New York, NY: Ballantine Books. Moseley J, Davis J. 1989. Psychological enrichment techniques and New World monkey restraint device reduce colony management time. Lab Anim Sci 39:31-33. Olson D, ed. 2004. Elephant husbandry resource guide. Fort Worth, TX: IEF. Parelli P. 2003. Natural Horse-Man-Ship: six keys to a natural horse-human relationship. Augusta, GA: Western Horseman. Poole J. Keynote address. 2001. EMA 22nd ann conf, Orlando, FL, October. Pryor K. 1999. Dont shoot the dog! The new art of teaching and training. New York, NY: Bantam Books. Reichard T, Shellabarger W, Laule G. 1992. Training for husbandry and medical purposes. Proc AAZPA ann conf. p. 396-402. Reinhardt V. 1992. Improved handling of experimental rhesus monkeys. In: Davis H, Balfour A, eds. The inevitable bond: examining scientist-animal interactions. Cambridge, UK: Cambridge University Press. p. 171-177. Reinhardt V, Cowley D, Scheffler J, Vertein R, Wegner F. 1990. Cortisol response of female rhesus monkeys to venipuncture in homecage versus venipuncture in restraint apparatus. J Med Primatol 19:601606. Videan E, Fritz J, Murphy J, Borman R, Smith H, Howell S. 2005. Training captive chimpanzees to cooperate for an anesthetic injection. Lab Anim 34(5):43-48. Whittaker M. 2006. Positive reinforcement training to enhance the care and welfare of captive animals. Paper presented at the joint mtg of Canadian Assoc Lab Anim Sci & Assoc Canadienne pour la Sci des Anim de Lab, Montreal, Canada, June.

Margaret Whittaker received her B.S. in Wildlife and Fisheries from Texas A&M, and completed masters work in Anthropology at the University of Houston. Her work with elephants began 16 years ago when she managed a breeding herd of Asian elephants in Protected Contact, including the first calf born into and trained in PC. In 1996, she began working for Active Environments (http://www. activeenvironments.org) as an animal behavioral consultant helping zoos, sanctuaries and biomedical facilities worldwide to develop behavioral management programs. Margaret may be contacted at 7651 Santos Road, Lompoc, CA 93436, at info@activeenvironments.org or at indu22@earthlink.com. Gail Laule received her masters degree in behavioral science from California State University, Dominguez Hills.She and Tim Desmond founded Active Environments to develop techniques to enhance the care and welfare of captive animals. For the past 15 years, Gail has created behavioral management programs for zoos, biomedical facilities and sanctuaries.She is also president of the non-profit organization, Wildlife in Need, currently engaged in conservation and animal welfare projects in the Philippines. Gail may be contacted at 7651 Santos Road, Lompoc, CA 93436, at info@activeenvironments.org or at moonshadowe@earthlink.net.
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Lisa F. Kane and Debra L. Forthman During the last 30 years, three innovative elephant institutions have emerged: one of them, in Kenya, rescues and reintroduces wild elephant orphans; the other two provide retirement alternatives for middle-aged circus and zoo elephants in North America. All three institutions focus on physical and behavioral rehabilitation and health. The David Sheldrick Trust Foundation has directed the Orphaned Elephant Project in Kenya for several decades. Its purpose is to rescue wild orphansoften infants suffering both physical and psychological traumaand to release them later into the wild as healthy and competent young adults. The Projects success has been remarkable. From the 1950s through the early 1970s, while David Sheldrick was Warden of Tsavo East National Park, eight orphaned elephants were released and successfully joined wild herds. Three among them are cows who have each had three wild-born calves since their reintroduction. Since 1987, 35 of the Trusts elephants who were hand-reared from birth and early infancy have been reintroduced into wild herds in Tsavo East. At the time of this writing, two of the cows are believed to be pregnant by wild bulls. Of 30 orphans who are presently keeper-dependent, 22 are in the process of rehabilitation, while eight remain in the Nairobi Nursery. The Performing Animal Welfare Society (PAWS), founded in California in 1980, and The Elephant Sanctuary in Tennesee, founded in 1995, provide alternatives to circus and zoo life for elephants in North America. The sanctuaries operated by these organizations share three important characteristics that strongly differentiate them from zoos and circuses: (1) each provides huge, varied spaces in which their resident elephants freely roam, browse and socialize; (2) the elephants are managed in the absence of human dominance, chaining, negative reinforcement or punishment; and (3) each program strives to maximize each elephants autonomy. Elephants at these two institutions typically arrive with health problems, some of them serious. Some have histories of lethal and near-lethal aggressive encounters with humans. In the course of dedicated efforts to rescue and heal elephants who have sustained injuries and insults to both mind and body, the directors of these non-public institutions have acquired a wealth of informationmuch of it surprising, some of it paradoxicalon both the enormous psychological and physical resilience of elephants, and the limits of these species ability to recover from both acute and chronic distress. Unlike some facilities, these three institutions do not share the mission to design optimal ex situ environments for healthy, prime animals; nor are they intended as research facilities for elephant breeding and training. In fact, while each operates in different ways, according to different personal philosophies, their directors are united in their single-minded dedication to making the complete well-being of each individual rescued elephant their primary agenda.

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Carol Buckley The Elephant Sanctuary in Tennessee The Elephant Sanctuary, operating on 2,700 acres near Hohenwald, Tennessee, is the nations largest natural habitat refuge specifically developed for elderly, ill or needy female African and Asian elephants retired from zoos and circuses. It is a nonprofit organization, licensed by the United States Department of Agriculture Animal and Plant Health Inspection Service (USDA/APHIS) and Tennessee Wildlife Resources Agency, and a member of The Association of Sanctuaries. Scott Blais and I founded the sanctuary in 1995 out of a concern for captive elephants fueled by our 35 years of combined experience in traditional elephant management. Our initial goal was to establish the sanctuary as an alternative to the traditional approach by creating an opportunity for solitary female elephants to live in a harmonious group of other similar females. Limits of traditional elephant management and exhibition Traditional captive elephant management is typically marked by human dominance, confinement in small, impoverished spaces and exhibition for our entertainment and education. Dominance is the traditional way that elephants have been managed for centuries. Human dominance over an elephant is attained through a variety of means: training, routine, positive reinforcement (reward), intimidation, deprivation, negative reinforcement (removal of an aversive form of stimulation) and corporal punishment. Dominance remains the standard approach today in nearly 50 percent of U.S. zoos and all circuses. Ron Kagan, director of the Detroit Zoo, aptly noted that elephants remain the only species in zoos that keepers are allowed to hit and chain. Traditional elephant management has done little to further an understanding of this species, instead serving mainly to enhance our ability to exhibit them. The limits of such a management tool are well described by Brambell (1973, p. 45): Often the approach to animal management in captivity has been to perpetuate, without searching for improvement, methods which allow the animal to survive long enough for its death not to be an embarrassment to the manager (as cited in Forthman 1998). Elephants have been exhibited in this country for over 200 years. Over these two centuries, however, conditions of their exhibition and confinement, like chaining, for example, have not changed appreciably. With the exception of certain progressive institutions, traditional elephant management programs continue to employ corporal punishment to manage their elephants. It is my perception that so long as dominance is considered a viable elephant management technique, negative reinforcement and corporal punishment will be defended as necessary tools of the trade.

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The Elephant Sanctuarys approach to elephant welfare and management The relationship between an animal, its physical environment and the occurrence of medical problems has been well-documented (Brockman et al. 1988; Munson & Montali 1990). Recognition of this relationship, provision of a spacious tract of undisturbed land and staff commitment to non-dominance and positive reinforcement have enabled the sanctuary to develop an elephant management approach that places elephant welfare as our highest priority. Passive control (non-dominance) and positive reinforcement The sanctuary staff does not use dominance as a means to manage our elephants. On a dayto-day basis, it is our experience that elephants respond favorably and consistently to positive reinforcement in the absence of dominance. The sanctuary has formalized its philosophy and employs passive control in the management of our elephants. This non-dominant technique utilizes the barn and yard facilities, caregivers knowledge of the individual elephant and positive reinforcement to encourage cooperation. No ankus, weapon, chains or form of negative reinforcement is used or permitted. Our elephants are requested to cooperate but no retaliation or negative reinforcement results if the elephant elects not to cooperate. Caregivers do not give our elephants commands. Instead, caregivers ask our elephants to comply. Patience and insight into how elephants solve problems are keys to a favorable response. Each elephant new to the Sanctuary has responded favorably to passive control. Our facilitys design and management philosophy permit our caregivers to shape our elephants behavior to suit the caregivers needs. Positive reinforcement in the form of treats, physical interaction and verbal praise are the tools of our day-to-day elephant management. Upon arrival at the Sanctuary, each new elephant is managed by passive control techniques within protected contact. Within a short time (sometimes within a few hours of arrival), each new elephant has cooperated in our system with. Because of the flexibility provided by the design of our barns and yards, we are equipped to modify our management of each individual in response to her behavior over the course of her lifetime. Currently, all but two of the Sanctuary elephants are managed using free contact with passive control. One individual has been identified as suffering from Post-Traumatic Stress Disorder (PTSD) and is currently being managed in protected contact with passive control. Several years ago, the sanctuary hired an elephant trainer versed in both free and protected contact management. The trainer, working in a protected contact environment, employed dominance as part of her training technique. One of our elephants immediately responded negatively. When the trainer approached this elephants stall, the elephant either was reluctant to cooperate or responded aggressively. However, when the identical training techniques were used without employing dominance (authoritative, demanding voice, withholding treats and interaction) the elephant was cooperative and showed no aggression. After some time experimenting with different training techniques and training personnel, we determined that this elephant was not responding adversely to the training itself but to what she perceived as human dominance. The stimulus that triggered the aggression was the attempted human dominance. In our experience, if an elephant is not dominated and we meet her basic needs for food, compatible others, a large space in which to exercise her freedom of movement and a sense of security, and she does not suffer from a psychotic disorder, she will be cooperative and non-aggressive.

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No chains In our experience, chaining is an unsound husbandry practice. Chaining adversely affects an elephants physical health by restricting mobility and potentially contributing to joint and bone disease. Chaining can be equally destructive to an elephants psychological health by preventing individuals from making their own choices and socializing in the complex way that ensures their psychological well-being. Modern facility design and our management philosophy alleviate the need for this archaic and detrimental tool. Housing options We have found that the application of innovative facility design coupled with a deeply intuitive management philosophy results in a high success rate of rehabilitation of captive elephants. Our facilities are designed to optimize each elephants quality of life. Knowing the species natural history and each individuals life story permits us to design and utilize facilities in a manner that maximizes the quality of their lives. Wild elephants spend their entire life outside, immersed in and migrating through a diverse habitat. It is our experience that in order to experience a full recovery, captive elephants must be afforded not only a diverse, vast area but they must also be given the freedom to make the choices that influence every aspect of their lives. Currently we have four on-site barns. Our goal is to provide safe freedom so that each elephant can recover and reclaim her true nature. The design process for each new barn contributed to our knowledge of available building materials as well as our understanding of how to achieve our goals, sometimes through unconventional means. We have abandoned traditional cinderblock walls for transparent polycarbonate sheeting that allows natural light to flood the barn. The heat captured from this innovative application of insulated plastic can be used to heat the barn. The barn roof is designed to funnel and capture thousands of gallons of rain water, which are used for cleaning purposes and to fill ponds. By providing not only interconnected interior stalls, but an auxiliary bypass chute which extends the full length of the barn, elephants can put as much distance between themselves and another elephant as they need to feel comfortable. Providing multiple options for accessing and exiting the barn is of primary importance. This option makes elephants feel safer and less restricted, thereby reducing stress levels and the incidence of intimidating overtures between non-bonded individuals. In our experience, the free-choice-access feature is most essential. Our new Asian Elephant Health and Welfare Institute/Quarantine facility is comprised of two barns on 200 fenced acres. The Phase I quarantine barn is a two-stall barn designated for medical treatment and quarantine. The Phase II quarantine barn is a six-stall barn designed for elephants whose health status is unknown, questionable, or for those who have successfully completed treatment for a transmittable disease. Our quarantine facility currently houses seven elephants with barn space for 11. The African facility has a five-stall barn on 300 fenced acres. It currently houses three elephants with barn space for five. The newly expanded Asian facility has a nine-stall barn on 2,200 fenced acres, with nine more interconnected stalls that create a chute the length of the barn. It currently houses seven elephants with barn space for 30 elephants. The land has a total carrying capacity of 100 elephants. To realize that population, additional barns would need to be constructed. Room to roam Elephants are migratory animals and require vast space to roam. The argument made by some that captive elephants do not need room to roam because keepers provide their basic needs of food, water and shelter is specious (e.g., Poole & Granli, Chapter 1). The provision of food, water and
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shelter addresses only a portion of an elephants needs and fails to take into account the psychological well-being of elephants. The sanctuarys 2,700 acres provide a protected, natural habitat for our three populations of elephants. All elephants have unrestricted, free-choice access to their habitats. Our observation is that given access to a diverse, vast space, captive elephants will engage in continuous activities consistent with their wild counterparts. We do not suggest that providing a healthy environment for captive elephants is easy; however, it is much less complicated than attempting to provide a healthy environment for elephants without adequate space. By following a comprehensive set of guidelines that addresses the physical, psychological, emotional and mental needs of elephants, the effort can be successful. There appear to be three key requirements for success; multi-hundred-acre diverse habitat where elephants are allowed to roam freely; free-choice access to lush and abundant species-appropriate vegetation; and social groupings of a minimum of five individuals. We are confident that the prototype we have developed can be utilized by others to improve captive elephant welfare. Live vegetation During the growing season at the Sanctuary, nearly 10 months of the year, 80 percent of our elephants diet is made up of the wild vegetation of their choice. Their access to a vast area to graze, browse and explore creates the opportunity for them to engage in this natural behavior much as they would in the wild, where they spend up to 20 hours a day selecting, collecting and eating their food (see Poole and Granli, Chapter 1). During the dormant season, our elephants derive only 30-40 percent of their diet from foraging. The opportunity to select, collect and ingest vegetation of their own choosing is an important aspect of any elephants life, captive or free. We have observed how painstaking particular elephants are when selecting their food. Each blade of grass is individually identified and harvested. The selection process takes concentration and patience. Elephants casually scan the vegetation with the tip of their trunk hovering over the area of choice, picking only a few pieces of vegetation from any one location. This continual highly selective process keeps them moving, always in search of greener pastures. Despite the fact that the elephants gather much less live vegetation during our few weeks of winter, we observe that their activity budget for grazing, foraging and exploring remains constant. Consequently, it is our perception that food gathering is only one of many factors causing them to forage and explore their physical environment and that they are deriving substantial psychological and social benefit from engaging in this natural behavior. Herd environment Our elephants are not related. Some have lived together for decades, others for only a few years. Their social needs drive them to develop relationships and strong bonds. The unfortunate fact that they are not related does not prevent them from developing deep attachments that mirror those of their wild counterparts. Room to maneuverto advance and retreat safelyhas a huge impact on an elephants social development. This ability to determine the degree of interaction an individual has with another is important for building confidence. Over time, even socially inept elephants can develop appropriate social skills, learning how to relate in a healthy way to other elephants and caregivers. The larger the herd, the more opportunities individuals have to bond. It is our experience that every elephant develops a strong bond with one other elephant and that this is their primary relationship. This special individual is the elephant that they rely on during times of insecurity and with whom they engage in play and exploration. Bonded individuals develop caring relationships with other members of the herd; their relationship is not exclusive, but it is the
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primary relationship in their lives. Freedom of choice Without freedom of choice in all aspects of their daily and nightly life, captive elephants fail to recover and discover their true self. When decisions are made for them, processed diets provided, or routines imposed which contradict their natural inclinations, elephants fail to blossom to their full potential. When they are allowed to make their own decisions, ones integral to their basic needsfood, water, friends and companions and activitiesthey build confidence, reduce stress and strengthen their immune system. This results in an ability to recover more easily from past trauma and to remain healthy. Decisions may be as sublime as when to take a drink and from what water source, when to nap, where and with whom, or what area of the habitat to explore. What is critical is that all of those decisions are made without human intervention. Not only do elephants heal rapidly in such an environment, most aggressive elephants do not feel the need to act out when they have the freedom of choice. Our elephants Who are our elephants? Tarra, our first resident, was the inspiration for the Sanctuary and moved in the day we purchased the land. Barbara was homeless when she came to us. She had been rejected by two breeding facilities and was living alone in her owners backyard. Jenny was next, crippled and living outside the jurisdiction of any regulatory agency that could protect her. It took us 16 months to get Jenny released to the Sanctuary. Shirley was not listed in any record I could find, but there she was, residing in a small zoo in the South. The zoo had kept her alone for 23 years and was overjoyed to learn about us. The zoo made arrangements to have Shirley moved within weeks. Bunny followed three months later. Bunny had spent more than 44 years alone in a small zoo in Indiana. The zoo management supported the move but the community was reluctant to let her go. Bunnys relocation was a five-year project for us. Bunny proved all the concerned zoo supporters wrong by bonding with all of the resident elephants within hours and leading them to the swimming hole for her first swim in 30 years. Next came Sissy. Sissy was a complete surprise. She was not living alone, and we were not informed that the zoo had any intention of moving her to us. The zoo called us in the wake of a public outcry following the disclosure of a tape showing Sissy being beaten by zoo staff. Six weeks later, Sissy became our sixth resident. Several months later, Winkie, an elephant that captured the medias attention when she injured a visiting veterinarian, was allowed to retire to the sanctuary. The arrival of these seven elephants was spread out over five years, enabling us to gain knowledge and confidence regarding our specialized work. Over the next five years, our property expanded from 100 to 2,700 acres, three separate multi-acre facilities were carved out of the habitat, two additional barns were built and our elephant population increased by 15. Instead of receiving a solitary elephant with minor physical problems, we were now engaged in multi-elephant rescues, many with serious physical and emotional conditions. In 2003 we rescued two elephants with terminal cases of osteomyelitis: Tina from a zoo in Canada and Delhi from the Hawthorn Corporation in Illinois. Delhis rescue was the first time that the USDA had ever confiscated an elephant. In 2004 we received Tange, Zula and Flora, our first African elephants, and Lota and Misty, two tuberculosis-positive elephants from the Hawthorn Corporation. Lota succumbed to her disease fewer than three months following her arrival. In January of 2006 we took custody of eight circus elephants. All had been exposed to tuberculosis.

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Eight of our elephants have documented histories of repeated acts of aggression toward keepers prior to moving to the Sanctuary. In all but two cases, these behaviors ceased after their move to the Sanctuary. All but one of the 22 elephants displayed stereotypical head bobbing and swaying upon arrival. In all cases the stereotypical head bobbing and swaying halted immediately when the individual was engaged in species-typical activities like walking, foraging and interacting with other elephants. Nearly half of the elephants that retreat to the barn for short periods of time at night display the stereotypical head bobbing and swaying while inside. Eighty-two percent of the elephants arrived at the Sanctuary with nail and foot pad problems, some of them life threatening. Foot health directly reflects the degree to which a captive elephants habitat is species-appropriate. Diseased feet remain the number one cause of death in adult captive Asian elephants. Without exception, each of our elephants had lived in a restricted space with little or no access to natural substrate. In one especially severe case, records accompanying the elephant indicated a 25-year history of chronic abscesses in every nail. After six months at the sanctuary, this elephants nails and pads were completely healed. She has been in residence for eight years and her feet remain healthy with minimal routine foot care. With the exception of osteomyelitis, all foot and nail problems have been remedied in a matter of months. Elephants that arrive with osteomyelitis receive care and treatment but we recognize that they are receiving hospice care as osteomyelitis has not yet been cured in elephants. Seven out of 23 elephants relocated to the sanctuary lived solitary lives prior to their arrival. One individual was solitary for less than a year, but others were solitary for most of their lives from 20 to 46 years. Without exception, each solitary elephant bonded with another elephant within 24 hours of their arrival at the sanctuary. Within our three herds (17 elephants in total at the time of writing), we have seven primary relationships and two functioning herds. The African herd, our only deficient herd size, has only three members, one of which is the individual identified with PTSD. Following a recent visit to the sanctuary, Katherine Payne, Director of the Elephant Listening Project, stated, Identical relationships of bonded individuals have been observed in herds of wild elephants. Some of the Sanctuarys elephants exhibit herd behavior identical to that of their wild counterparts. Conclusion The Elephant Sanctuary has existed for 13 years, overseen by a staff with 65 years of combined experience in captive elephant management. Aggressive elephants have moved to the sanctuary and their aggression has subsided. Elephants plagued with foot health problems have moved to the sanctuary and their feet have healed. Elephants with stereotypical behavior have come to the sanctuary and over time, their compulsive bobbing and swaying have been replaced with species-typical behaviors. Elephants who have lived their entire captive lives in isolation retire to the Sanctuary and bond with other resident elephants within hours. What we have learned at the sanctuary can be applied to the management of other captive elephants. For those elephants with behavior and physical problems that prevent them from thriving in a traditional exhibit environment, an alternative is available.

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References

Brambell MR. 1973. The requirements of carnivores and ungulates in captivity. In: The welfare and management of wild animals in captivity. Potters Bar, UK: Universities Fed Anim Welf. p. 44-49. Brockman DK, Willis MS, Karesh WB. 1988. Management and husbandry of ruffed lemurs (Varecia varigata) at the San Diego Zoo. 3. Medical considerations and population management. Zoo Biol 7:253-262. Forthman DL. 1998. Toward optimal care for confined ungulates. In: Shepherdson DJ, Mellen JD, Hutchins M, eds. Second nature: environmental enrichment for captive animals. Washington DC and London, UK: Smithsonian Institution Press. p. 236-261. Munson L, Montali RJ. 1990. Pathology and diseases of great apes at the National Zoological Park. Zoo Biol 9:99-105.

Carol Buckley has over 30 years of experience in the care and management of Asian and African elephants. In 1995, Carol co-founded The Elephant Sanctuary in Tennessee, the nations first natural-habitat refuge for sick, old and needy endangered Asianand African elephants. Carol and her staff have built an organization that has rescued 23 elephants and has over 73,000 members. Carol was honored for her innovative work by the 2001 Genesis Awards and as A Hero For The Planet by TIME magazine. She has been the subject of recent features in The Chicago Tribune, People, The New York Times Magazine, and CNN, and has authored two childrens books on elephants. Carol attended the Exotic Animal Training and Management Program at Moorpark College in California, and is licensed by the United States Department of Agriculture and the Tennessee Wildlife Resources Agency. She is a well-known speaker on the subject of elephant care. She may be contacted at P.O. Box 393, Hohenwald, Tennessee, 38462 or at carol@elephants.com or at http://www.elephants.com.

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Pat Derby Director Performing Animal Welfare Society

The information contained in this chapter is purely anecdotal and reflects my personal experience during 15 years observing captive elephants in substandard environments, chained and trained by extremely inhumane methods, and 20 subsequent years attempting to create a social and biophysical environment to improve the physical and psychological health of the elephant residents at the Performing Animal Welfare Societys (PAWS) sanctuary for captive wildlife in Galt, California. Our struggle to improve conditions for these elephants has given me an insight into the very complex issues of captive elephant welfare, and I am apprehensive about the current perception that moving elephants to a sanctuary automatically improves their physical and psychological health. It is disingenuous to assume that all zoos are bad and all sanctuaries are good. After spending 35 years with captive elephants, I am convinced that elephant capture and subsequent captivity cause irreparable and irreversible harm to individual elephants (see Bradshaw, Chapter 4), and that captive breeding programs are ethically irresponsible. Nomenclature has influenced the frenzy to breed endangered species in captivity; designation of endangered habitat as a conservation tool might have improved captive elephant welfare. Decades of careful and systematic field research by scientists substantiate my own empirical conclusions that elephants are highly sensitive, intelligent animals who rely on an intact, functioning social order to prevent stress and maintain normal physical and mental health (see Poole & Granli, Chapter 1; Lee & Moss, Chapter 2). Most captive elephants were born in the wild and captured when they were infants or young juveniles. Asian elephants were driven into large stockades where mothers and infants were separated and the infants brutally broken and trained, while African elephants witnessed the mass slaughter of their families; all captive elephants have endured the trauma of transport to an unfamiliar place populated by strangeor noelephants, and humans. In the course of their lifetime, they may have been moved from one location to another, repeating the same patterns of distress and further increasing the possibility of aggressive, antisocial behavior. Captive elephants frequently live in dysfunctional groups of unrelated individuals with stronger, more aggressive (dominant) females vying for control. There are no traditional herds or matriarchs, no long migrations for food, water or breeding opportunities. Further, and perhaps most importantly, all captive elephants are managedusually in inadequate facilitiesby an eclectic group of humans who cannot agree on basic standards of care. Captive elephants suffer from a lack of traditional elephant social systems, and often compensate by forming bonds with one or two compatible elephants. They rely heavily on routine, and changeeven for the bettercan cause distress. The removal of an individual elephant from familiar surroundings and
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companions is a highly traumatic experience that can cause physical and psychological problems and, occasionally, death. Psychological problems exist in all captive elephants to some degree, and careful monitoring of the individual elephants behavior is necessary to prevent injury or death to other elephants, keepers and handlers. The assumption that providing space, habitat diversity and elephant companions is a panacea for the many physical and psychological problems that plague captive elephants is a dangerous and far too simplistic solution. Profound disruptions in routine and changes in environment can cause trauma to individual elephants despite our best efforts to improve their quality of life. Proposed elephant moves should be cautiously planned and alternative solutions explored before a final decision is made to relocate an elephant. If removal of an elephant is deemed necessary to improve her quality of life, all involved should evaluate the elephants physical and psychological condition carefully, and planning should commence in order to begin to alleviate the stress of moving and socialization with other elephants and humans. Some elephants adapt readily to change, especially those involving an improved environment; others may not respond as quickly. Adjustment periods vary with individual elephants; integration and socialization is never successful until issues associated with the individuals history are resolved. At PAWS, we describe this adjustment period as going on elephant time, which means that we provide the space, freedom of choice, diversity of habitat and companions to encourage socialization, then we monitor activity for changes in behavior. Monitoring involves constant observation of behavior changes that occur when individual elephants are integrated into the group. I often sleep in the elephant barn during these periods, and we maintain a 24-hour keeping staff. Subordinate individuals are easily identified by submissive body language and vocalization and the cautious manner in which they approach other elephants, usually backing into the group and retreating whenever signs of aggression like pushing and shoving are displayed. It is not our policy to force socialization of individuals who may not be compatible or to stress subordinate elephants by placing them in close proximity to overly dominant elephants. While others may disagree, we have found that some dominant elephants will pursue and harass a subordinate elephant no matter how large the space. PAWS elephant program began in 1985 with one tiny infant elephant, number 71 in a group of 86 elephants orphaned by a cull in Zimbabwe. By that time, hundreds of juvenile African elephants, orphaned by culls, were flooding into this country to be used as attractions at zoos, circuses and other public displays. The practice of culling, the systematic killing of large family groups of wild elephants to control population, was the accepted solution to Africas problem, but it created a greater disaster by providing infant elephants to animal dealers and others for a tidy profit. Seventy-one, like many others, was a neurotic four-year-old infant, underweight and malnourished at 487 pounds. She was not expected to survive when we brought her to PAWS. After years of watching trained elephants languishing in chains, my partner, Ed Stewart, and I vowed that 71 would never again be chained, cruelly trained, poked, prodded or punished. We did not rename her, hoping that we would be questioned about the origin of her name and the reason for the number. While zoos were promoting captive elephant breeding programs to save the species, we were watching with dismay the hundreds of orphaned infant elephants pouring into this country for entertainment. Our Galt sanctuary was a 30-acre former dairy which we had converted to a tree-lined refuge for lions, tigers, bears and other abused and abandoned captive wildlife. When the infant elephant 71 arrived, we established a management routine, which provided grassy, fenced enclosures where 71 could graze, walk, dust, mudbathe and browse with human companions to protect and care for her. She was never alone, as one of us was with her 24 hours a day; she was never chained or
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punished, and daily care was accomplished by food reward and the natural bond that develops between any infant animal and her principal caretakers. In the following five years her health improved and 71 grew to be a strong 3,500 pounds. In 1990 we brought Mara to the sanctuary. Mara, considered a wild and very dangerous African elephant, was nine years old, the same age as 71. We had previously assisted in Maras rescue from life in a Mexican circus and had arranged to send her to a millionaires 800-acre horse ranch in Florida, which housed the Zimbabwe cull elephants and, at that time, 71. An agreement was made between the owner and PAWS that ensured Maras future return to us when he decided to disperse the elephant herd. Once again, Mara was saved from life in the circus. The Florida facility housed over 90 juvenile African elephants, 86 from the Zimbabwe cull and 8 or 9 from previous culls. The elephants were separated into compatible groups and roamed, unchained, in spacious areas with caring keepers. Despite his benevolent purpose, however, caring for over 90 wild elephants soon became too much of a commitment for the wealthy entrepreneur, and the juvenile pachyderms were sold to animal dealers all over the country. We received tearful telephone calls from their keepers as the wild young elephants were tranquilized, chained for the first time in their lives, and loaded into trucks to be sold as performers for public amusement. Mara had been living in a cohort of 20 for four years, the constant companion of the dominant female. After a three-day journey by truck, she arrived at PAWS bellowing and charging at 71 and every human who came within 50 feet of her enclosure. Maras obvious distress and confusion at the loss of her elephant companions and the change in her physical environment provided our first experience with re-socialization and adjustment between unrelated elephants with different histories and social attachments. Mara had been captured in South Africa as a weanling and sent to a petting zoo in California. At an age when infant elephants forage constantly and enjoy the attention of a herd of doting adults, she was alone, on display, and fed primarily by the public from vending machines filled with grain or peanuts. Since she ate only when visitors fed her, she had developed behavioral problems associated with feeding, racing around her small paddock whenever anyone approached the vending machine. Her food anxiety was further exacerbated when she was transferred to the Florida facility to live in a large group of wild elephants and compete for food. Maras food issues have become an integral part of our management program. The socialization process for the two young African elephants took almost six months. We built stalls and corrals with common walls to allow physical contact between the two behind protective barriers. Initial contact was tentative and both elephants feigned indifference most of the time. A positive benefit resulting from our close relationship with 71, was Maras acceptance of our presence. After weeks of bluff charges, foot stomping and head shaking, the two began to touch and rumble with pleasure; finally, we removed the barriers and held our breaths. Amid a cacophony of rumbles, trumpets, bellows and squeaks, the two urinated and defecated, touching trunks to temporal glands and mouths and bonding for life in a ceremony that was profoundly moving. As 71 and Mara grew, new construction followed and new management practices evolved. Our plans to provide the two young Africans freedom from pain, fear, chains and punishment became untenable at times when their juvenile pranks and boisterous antics appeared uncontrollable to elephant handlers from traditional institutions who were critical of our lenient approach. We had our own doubts about the outcome, but never wavered in our determination to maintain our captives in an enriched environment. Our physical facility supported a 5,000-square-foot barn and a two-acre natural substrate enclosure filled with trees, grass, bamboo and a lake. The elephants spent their days swimming, bathing, mudbathing, browsing and grazing. We managed them with food reward and distraction,
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and both elephants responded positively, following buckets of treats when we led them into the barn or out into the habitat. They were never restrained and freedom of choice prevailed in all their activities. Seventy-one displayed no neurotic behavior, and Maras food issues were addressed by feeding her first; this seemed to work to the satisfaction of both elephants. At that time, it was inconceivable within the elephant management community to manage elephants without the use of an ankus (bull-hook). The ankus is described by those who use it as a guide, but it is actually a weapon designed to punish misbehavior. At this point our only concern was providing a decent place to live to the two young elephants who we felt were victims of captivity; there was no thought of formalizing the program which we had initiated of necessity and not as a scientific experiment. I had worked with elephants for over 20 years and my own respect for what is, in my opinion, one of the most intelligent creatures on the planet, precluded my ability to function in a traditional free contact environment where punishment is used to discourage unacceptable behavior. I never used an ankus or other punishment in dealing with elephants because I was incapable of such actions. I dealt with elephants on their terms and had the good sense or instinct to stay out of their way if they were aggressive. When Protected Contact management was first presented in 1991, I was elated to hear that an alternative method of management and training for elephants based on positive reinforcement had evolved after a particularly cruel training session at a popular zoo had evoked a firestorm of public outrage. Ed Stewart, my partner, shared this philosophy. When I met Ed, a graduate of the University of Tennessee with a degree in communications, he had no experience with animals, but he did have an innate understanding of their right to exist on their own terms. As he worked with me and began to learn about the complexity and diversity of the various species of animals in my care, his convictions became as strong as mine. It should be clearly understood that, in our opinion, no captive situation can ever replace the wild; captivity foments insoluble problems for elephants and those who care for them. Providing care for the two young elephants triggered our own involvement in the issues raised by keeping elephants in captivity; we were convinced that elephants were a species that should not be kept in captivity. Reading studies by researchers in the field and their accounts of wild elephant behavior and social structure left us with an overwhelming sense of inadequacy and frustration. In 1995 we created our own litmus test when we agreed to accept two aging Asian elephants from the Milwaukee Zoo. When Tammy and Annie arrived and we removed the chains from their legs for the last time, we knew we were committed to a program that was necessary but that, in our opinion, could never be ethically or morally justified. The addition of Tammy and Annie to our elephant population presented an even greater quandarythe need for assistants to help us care for our expanded group of elephants. Safety concerns were obviously an issue in working closely with elephants as we did with 71 and Mara, and we were not prepared to expose others to the dangers inherent in free contact elephant care, especially without bull hooks. Thus began our involvement with Protected Contact Management (see Whittaker & Laule, Chapter 13) and the benefits to both elephants and keepers of a concise program based on the elephants needs and engaging their cooperation without punishment or retribution. With the exception of 71, the elephants now kept at our second sanctuary, ARK 2000, arrived with foot abscesses and other problems related to standing on unnatural substrates, often chained for long periods of time; these and degenerative joint disease are physical conditions that must be treated and observed constantly. Although an improved environment is a major factor in alleviating these problems, treatment is often necessary as well. We have remained committed to Protected Contact as a management practice and our staff of nine supervisors and keepers trim feet that require constant care after many years of standing on
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concrete, and medicate, monitor, feed, bathe and move the elephants at ARK 2000 from behind protective barriers. All of the elephants enjoy the game, even when it involves some discomfort. When the elephants are in the habitat, distance becomes our barrier, and keepers move the elephants to the barn utilizing recognizable treat containers and whistles that allow the keepers to maintain a safe distance from the elephants at all times. We do not attempt physical exams, foot care or veterinary treatment until the elephants are inside the barn, and keepers are not allowed close physical contact with elephants in the habitat. Our elephants, particularly the young Africans, are excited and active when they are in the large areas. Conditioned to come to the barn for treats, the elephants eagerly anticipate foot and veterinary care as special times when they are pampered and coddled in close contact with keepers. The keepers access all areas of the habitat from outside roads, then go on foot into the habitat. Motorized vehicles are not permitted within the habitat when elephants are present; we have found that anything mechanical triggers excitement in our elephants and could create a potentially dangerous situation. Giving elephants sufficient space to express natural behaviors can create hazardous situations for staff. We are constantly changing protocols when new elephants arrive and have to adjust to expanded habitats and strange companions. After Tammy and Annie arrived in 1994, we designed and constructed the two-acre Asian elephant enclosure at the old sanctuary in Galt with a 4,000-square-foot barn where keepers could care for the elephants behind protective barriers, a ten-foot deep swimming pool, and grassy, natural substrate in the tree-lined habitat; these provided the two arthritic elephants with more diverse activity than they had known in 40 years. Despite the drastic improvement in their environment, both elephants were suspicious of the spacious, grassy yard and Annie was actively aggressive toward Ed and me. The two elephants had been brutally trained with block and tackle, electric shock and bull hooks, and both suffered from arthritis and foot and joint problems. They were suspicious and fearful of unfamiliar people, and their silence was a clear signal of stress. They had lived in an antiquated facility, chained on cold, wet concrete during long, harsh winters where environmental enrichment consisted of tropical murals painted on the walls. The dominant elephant at the zoo had devised her own escape from boredom in the relentless pursuit of Tammy, whom she knocked into the moat on several occasions. Our expectations of a positive reaction by the two elephants to a greatly improved environment diminished as we observed their obvious distress when confronted with radical changes in their daily routine. Tammy, who had been dubbed brain dead by her keepers at the zoo, was actually very intelligent, but, like many traumatized elephants, retreated into a shell as a form of mental escape. After years of abuse, Annie, who was devoted to Tammy, was dangerously aggressive to humans (see Bradshaw, Chapter 4). Necessary foot care and medical treatment were a challenge for the first six months; then, slowly, normal behaviors and vocalizations began to develop as the two responded to food reward and positive reinforcement with verbal encouragement and an enriched environment. The first time the two elephants actually played in their mud wallow, slipping, sliding, trumpeting and squeaking, was a joyful occasion for all of us, especially our veterinarian, Dr. Gai. Tammy still stood and rolled her head if Annie strayed too far away, but the familiar and chronic neurotic behavior that we had observed when they first arrived had decreased substantially. The two African elephants showed no interest in the new Asian elephants, although Tammy and Annie occupied an adjacent area. For several years, the African and Asian elephants at PAWS refrained from any audible communication, often ignoring rumbles and loud trumpets from the neighboring pair. There was no herd activity; the two bonded pairs remained detached.
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Minnie and Rebecca, two circus elephants, came to PAWS in 2001. We tried initially to socialize the new Asian elephants with Tammy and Annie, who were approximately the same age, mid-40s, but soon realized that Tammy was terrified of Minnie, the dominant female of the circus pair. Tammys fear of Minnie triggered a recurrence of her head bobbing and swaying whenever the two were in close proximity, but Annie eagerly approached the two elephants, seeming to relish the prospect of new companions. Both Minnie and Rebecca had been characterized as dangerous and difficult to manage and we kept them in a separate quarantine area when they first arrived. Rebecca, who appeared thin and lethargic, tested positive for tuberculosis during her first physical exam, so she and Minnie were kept in quarantine for one year while we treated Rebecca. Initially, Rebecca had no appetite and slept constantly, refusing all food and avoiding contact with people. Her successful treatment and subsequent recovery is a testimony to the positive effect of an enriched social and biophysical environment and her strong bond with Minnie. After years of searching for a larger property, we acquired 2,300 acres of rolling hills and oak forests in the foothills of northern California where we immediately constructed a 100-acre natural habitat for our four Asian and two African elephants. We knew space was an important component in elephant welfare, but we had no practical experience to guide us in choosing the size of the habitats. We allocated a 75-acre habitat of steep hills, heavy vegetation and a 20-foot-deep, five-acre lake for the healthy and spirited African elephants, while designating 35 acres of gently rolling hills and ancient oak trees for the older, physically challenged Asian elephants. Since we were still treating Rebecca for tuberculosis and Tammy was much too frail to travel, we decided to move the Africans to their expanded habitat first. Trailer training for the two elephants, who had never left the property since their arrival as juveniles, took three months using food reward and positive reinforcement, which often consisted of verbal encouragement and rumbles and squeaks from the trainers when the elephants entered the trailer and calmly ate their treats. We rode inside the trailer with the elephants during the trip and observed the stress that transport can cause, even under the best of circumstances. For 71, who had never been chained or closely confined, the short trip was a frightening experience and she rejected all of our attempts to calm her, refusing her favorite food treats and ignoring our verbal encouragements. The new 20,000-square-foot barn with large, heated stalls and the huge African elephant habitat with the lake, trees, grass and hills to climb was our dream for 71 and Mara. We anticipated excitement and pleasure from the two elephants who, much to our dismay, stood quietly, ears out, one leg raised, listening. In the ensuing weeks, they did not explore, only moved about when we went with them, and stood constantly with one foot raised and ears flared. We soon realized that they were listening for the familiar sounds of the old facilitythe Asian elephants, the lions and tigersall the comforting sounds of an environment that they had known for years. We had disrupted their routine, drastically altered their physical environment and, despite all our lofty plans, had traumatized two elephants who were secure and comfortable prior to the move. Their adjustment to the improved environment was a slow process that supported our hypothesis that elephants often react negatively to change. Today, the two elephants climb the hills, swim in the lakes and forage and browse, benefiting from the expanded environment; but the adjustment time was an unexpected and critical part of the ultimate psychological improvement. Older elephants with physical disabilities may not survive a long, traumatic period of adjustment. Because of the risk of jeopardizing 53-year-old Tammys already failing health with a move, the Asian elephants remained at the old facility until her death in 2003. Familiar as we were with the depth of the bond between Tammy and Annie, we were unprepared for the enormity of Annies grief at the loss of her companion. Our own devastation paled
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in comparison to the palpable suffering of Annie. Elephants, I believe, have a ritual of death that involves their closest companions; it is an acceptance of release from physical pain and a vocalization that indicates their passing. Tammy had fallen down twice before and Annies frantic attempts to raise her often interfered with our own efforts; this last time, Annie stood quietly touching her friend with her trunk as they both rumbled softly, then walked away to the farthest corner of their yard and stood watching as we tried to get our beloved elephant back on her feet. We knew from Annies behavior that Tammy was dying. Annies grief was a most graphic demonstration of elephant attachment and social bonding; she was not aggressive, but simply stood quietly in the spot where Tammy died, refusing to move and eating very little. Preparation began immediately for her transport to ARK 2000 where we hoped the company of Minnie and Rebecca and the new habitat would alleviate her suffering. Our veterinarian, Dr. Gai, had arranged an extensive necropsy on Tammys remains at the University of California, Davis, and the results showed Tammys death was caused by degenerative joint disease. We were pleased to hear that eight years of standing on soft dirt and grass were very beneficial to her feet and had probably prolonged her life by several years. However, 40 years of standing in chains could not be undone and ultimately led to her death. Information gleaned from necropsies is essential to solving health problems in captive elephants; necropsies should be mandatory in every elephant death. It is irresponsible for any facility to neglect this important aspect of health care and management. We moved Annie, Minnie and Rebecca to ARK 2000 soon after Tammys death. The interior of the Asian elephant barn was unfinished, so we divided the huge African barn into two sides separated by a long hallway, which was designed for socialization of new elephants. When the Asian elephants arrived, the reaction of the African elephants was surprising after their indifference at the old facility; they rumbled loudly, bowing and stretching, urinating, defecating and trumpeting. We slept in the barn with the elephants until the Asian barn was completed, and the vocalizations among the group vibrated through the barn each night as one elephant, usually an African, would begin to rumble until the entire group joined her with low rumbles and high-pitched squeaks from the Asians and an occasional trumpet from Mara. Elephants do mimic sounds. Minnie imitated a sound that resembles the clicking of a dolphin. Seventy-one had learned this from Mara, and the two Africans engage in it when they are eating or drinking. Minnie now makes the sound just before treats are distributed, imitating the Africans vocalization perfectly and in a context that seems to indicate sensory pleasure. Minnie and Rebecca adjusted quickly to their enlarged habitat: climbing hills, swimming in the lake, dusting and mudbathing. Rebeccas health improved as she gained muscle tone and weight; further, the stereotypic swaying, which is a trademark of captive elephants who have lived in chains, was observed less frequently. Annie continued to grieve for her lost companion for more than a year after the move. She stood by the gate every morning, and then returned to the barn. Her only real pleasure was the indoor Jacuzzi that Ed had designed for Tammy. When older elephants cannot lie down to rest, it is critical to provide a pool or a large dirt mound to alleviate the constant pressure of their weight on feet and joints. Annie had no problem lying down in the old facility, but she refused to lie down in the new barn and habitat, so we would coax her into the Jacuzzi where she slept floating in the water. Annie spent time with Minnie and Rebecca in the barn, but remained alone when they ventured into the habitat. Annies decision to end her period of mourning occurred suddenly on a beautiful summer day as she stood in the same spot by the gate waiting to return to the barn. Just as we opened the gate and she began the climb up the hill, she stopped and turned around, then raced down the hill into the habitat and on into the lake. She spent the
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day exploring with Minnie and Rebecca. Today, she is our most active Asian elephant, covering the 35-acre area at least once a day, swimming in the lake and sleeping in the sun on her favorite hill. Other elephants who have come to ARK 2000 include Winky and Wanda, a bonded pair of Asian elephants from the Detroit Zoo, who were sent to our facility to escape harsh winters. Wanda astounded us, and her keepers who traveled with her, when she sauntered out into the habitat, vocalizing and displaying all the proper greeting postures to Minnie, the dominant female of the Asian group. It has been our experience that subordinate females have less difficulty in adjusting to new environments than dominant females, but Wandas rapid acceptance of her new surroundings was a pleasant surprise. Subordinate females seem to have less need to control while dominant females are inherently compelled to challenge other dominant females. Although Wanda adjusted immediately to her enriched social and biophysical environment, Winky had difficulty in establishing her own routine, and distrusted and feared her new companions, particularly Minnie. At 54, her age is another factor in our evaluation of her ability to adjust to new elephants; therefore, she is given the choice of spending time with the others or avoiding contact. Before Winky and Wanda arrived, we decided after considerable research to provide dirt floors for the older, arthritic Asian elephants. This decision, made with some trepidation, was made to relieve the trauma of standing on hard concrete surfaces when the elephants stay indoors. Although we had calculated the physical benefits of dirt floors, we did not anticipate the psychological effects. A large proportion of the time our Asian elephants are indoors is spent dustbathing and digging in the dirt. Our greatest challenge in integrating new elephants into an existing social system came with Lulu, a 38-year-old African elephant who had lived for 34 years with an overly dominant 46-year-old cow, Maybelle. According to reports from keepers, Maybelle would hold Lulu down and prevent her from moving, push her out of the barn and into the moat, block her way to food and anything else that she wanted, precluding her ability to make any choice without the express permission of the older elephant. This excessively dominant behavior, which I understand is nonexistent in wild elephants, is often seen in captive elephants, especially those who live in pairs. Lulus past experience with only one other elephant companionand an abusive one at thatseriously hampered our ability to introduce Lulu to 71 and Mara. Her overly submissive behavior, including dog-like squatting whenever the two elephants approached, triggered excitement and apprehension in them. Neither elephant appeared aggressive, but Lulus distress, squatting when she felt trapped, was alarming to us. Our management plans for the three Africans have included escape routes for Lulu, allowing her to retreat to a fenced-off area or to her individual stall in the barn. Lulu had also developed the habit of throwing feces on herself as a replacement for dirt and mud, which was lacking in her old enclosure. Her discovery of mud holes and dirt for dusting eventually minimized her unpleasant behavior, but frustration often triggers a recurrence. When Ruby, a 47-year-old African elephant from the Los Angeles Zoo, arrived in May 2007, she had an immediate and profound impact on the group. We positioned her on the side of the barn opposite 71 and Mara, sharing a common wall with Lulu, the subordinate elephant. Ruby, who was accompanied by some of her keepers from the zoo, was quite complacent about her new surroundings, moving about the barn and calmly stretching her trunk out to the other elephants. Lulu was excited and curious about Ruby, displaying none of her usual subordinate behavior; indeed, she appeared confident, almost imperious, attempting to establish dominance over Ruby. We were somewhat disconcerted because Rubys reputation as aggressive to people and other elephants had preceded her. Before coming to PAWS, she was sent to Knoxville Zoo, where attempts to socialize her with other elephants were unsuccessful. She had attacked the dominant
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elephant in that group and chased a keeper from the yard. A year later, she was sent back to Los Angeles where she lived alone until her transport to ARK 2000. We expected the elephant hierarchy after Rubys arrival would continue with Lulu at the bottom and 71 and Ruby vying for top position. The next day, it was apparent that Lulu had finally found an elephant who would allow her to be dominant. After years of suppression, Lulu was insufferably domineering to Ruby, throwing her trunk over Rubys head, mock charging and blocking Rubys passage out of the gates. Ruby, who is built like a tank and could have squashed little Lulu with one blow, calmly tolerated Lulus uncharacteristic behavior, backing into her when she blocked the way and accepting with deference Lulus premier attempt to dominate at least one other elephant in her lifetime. We will never know why Ruby behaved so graciously to Lulu, but her presence in the group actually created the balance that was lacking when 71 and Mara were with Lulu. Rubys behavior with the other two African elephants was quite different; she knocked Mara down and chased 71 on some of the initial introductions, but both 71 and Mara were quick to initiate subordinate behavior, avoiding further confrontations. These four elephants, all with different histories, are now one cohesive group, standing butt to butt, rumbling, touching trunks and occasionally sparring under the tall oak trees, then shuffling across the dry grass, pushing through brush and throwing dirt, exploring their expanded habitat and exhibiting behaviors that we hopefully construe as natural in their endearing attempt to create a herd. Two recent additions to the rapidly growing elephant population at PAWS are Nicholas and Gypsy. Nicholas, a 14-year-old Asian bull, was born in captivity and separated from his mother before he was two years old. He was riding a tricycle and performing in a circus at that age, and retired when he became difficult to manage at age five. He lived with Gypsy, an unrelated Asian female, who has been his constant companion for the past nine years. The two had lived together in a single stall until their transfer to PAWS Galt facility where they must live in quarantine for at least one year. This unusual coupleGypsy is 40is a remarkable example of the resiliency of the elephant spirit and their inherent need for lasting social relationships. Although we cannot predict how they will behave as Nicholas matures, at present, it would be cruel to separate the two who have managed to survive because of their bond. They are inseparable, moving in tandem across the yard, bathing, mudbathing and playing, never straying too far apart, rumbling, squeaking and trumpeting when they are reunited after a short separation for baths or foot trims. African elephants are quite different from Asian elephants; they are more active, energetic and tenacious; and captive elephants bear little resemblance to their wild relatives. Our experience with raising an infant elephant in captivity has taught us much about their intelligence, loyalty, complex social system and their need to have choices and control of their environment. Because we provided these key welfare components, 71, at 26 years of age now, is probably the least neurotic elephant in captivity, and the comparison between her behavior and physical health and that of the other elephants in our care provides the best argument in favor of enhanced social and biophysical environments for raising orphaned elephants in captivity. The argument still exists against keeping elephants in captivity and we are supportive of that position; however, we have found that, with time, patience and informed decisions, changes in the social and biophysical environments can yield improved physical and psychological health for captive elephants. Standards of care should be initiated to mandate improved conditions for captive elephants. Our conclusions are based on our experiences over 35 years as we have researched and created
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a sanctuary for captive elephants: 1. Captivity cannot replace the wild; therefore, capture of wild elephants should be prohibited. 2. Until there is a comprehensive plan for lifetime care, intact social systems, and provisions for greatly enhanced biophysical and social structures that promote and stimulate herd activity and development, captive breeding should be prohibited. Captive breeding, particularly through artificial insemination, to date has produced neurotic, aggressive calves, born with the mother chained and without the presence of the mothers companions; these young ones are even less equipped to deal with captivity than those born in the wild. 3. Facilities that house the victims of captivity should provide the space, and complexity and diversity of environment that encourages social interaction and natural behaviors, and decreases health problems. Natural substrates, space and positive social interactions are critical to improving the health of captive elephants. 4. Attention should be given to the needs of individuals, increasing their opportunities for choice and control. 5. Management techniques that rely on dominance and physical control of the elephant should be prohibited. 6. Necropsies should be mandatory to provide important information for health care research. 7. Alternative plans should be considered before removing old or terminally ill elephants from familiar surroundings. Often, changes can be made that will enhance their quality of life without resorting to the stress of transport and the trauma of adjustment to new surroundings and companions. 8. New standards of care for elephants and safety for keepers should be developed that include provisions for maintaining elephants in large habitats and larger social groups. In my opinion, management of captive elephants is a work in progress, and failures are as important as successes in creating enhanced social and biophysical environments. We are all exploring new ways to improve the quality of life for animals who do not belong in captivity; sadly, our best can never be enough. Pat Derbys advocacy for animals began over 35 years ago when she started work with wildlife in the entertainment industry. The Lady and Her Tiger, Pats expos of the treatment of performing animals, won an American Library Association Award in 1976, the year Pat met Ed Stewart; they formed PAWS in 1984 and moved to Galt, California in 1985. Because of the critical need for experienced care-providers for abused and abandoned captive wildlife, PAWS opened the Galt sanctuary. Pat has testified before Congress and served on state committees to develop standards of care for elephants and other exotic species. Pats second book, In the Presence of Elephants, was published in 1995. In 2000, PAWS purchased 2,300 acres in San Andreas, California, and established ARK 2000, their second wildlife sanctuary. In 2005, Pat received a Lifetime Achievement Award from In Defense of Animals, an international animal welfare organization. In 2005, she received the Sacramento SPCAs Lifetime Achievement Award. She may be contacted at PAWS, Performing Animal Welfare Society, P.O. Box 849, Galt, CA 95632, at http://www.pawsweb.org/ or at patderby@pawsweb.org.
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Chapter 16 The Rearing and Rehabilitation of Orphaned African Elephant Calves in Kenya
Dr. Dame Daphne Sheldrick, DBE, MBE, MBS, DVMS David Sheldrick Wildlife Trust Working with elephants for 50 years of my life has been an exceptionally enlightening and fascinating experience which has opened an intriguing window into the elephant mind. Elephants are emotionally very human animals, sharing with us the same emotions that govern our own lives, plus an identical age progression, the same sense of family, sense of death, loves and loyalties that span a lifetime, and many other very human traits, including compassion. They have also been endowed with other attributes we humans do not possess, such as innate knowledge in a genetic memory, something we humans vaguely term instinct, which becomes honed by exposure to a wild situation. However, in such a long-lived species, there is also a lifetime of learning through experience, just as there is for humans. The nursery stage The most important thing in the world to a baby elephant is its mother and extended family. Orphaned female elephants are particularly vulnerable to psychological despair after having lost their natural family. Young bull orphans are more resilient, mainly because female family members will be bonded together for life by emotional attachments that are lasting and strong. Young bulls normally leave their natal family at puberty, preferring the company of other young bulls and emulating the example of high-ranking dominant males within the elephant society. In infancy, the family lost to the orphaned elephants must be replaced by a human equivalent. The successful rehabilitation of African elephant calves back into the wild community when grown begins during the Nursery stage, the first two years of milk-dependency; it is essential to nurture the psychological aspect of a baby elephant as well as the physical so that it will be accepted into a wild community. Wild elephants will not wish to take on a calf that is mentally unstable due to incorrect husbandry whilst young. The psychological aspect of hand rearing elephants is as crucial as everything else. Human elephant keepers must replace the lost family to be with the babies 24 hours a day, traveling with them as a group during the day and sleeping alongside them within their stable at night, in physical contact at all times. Keepers sleep with a different elephant each night to avoid any strong attachment to one person, which can prove counterproductive should that person become absent for any reason. Elephants are tactile and highly social animals, so the human family is encouraged to fondle the babies gently, demonstrating heartfelt affection, as would an elephant family. Elephants can read a persons heart, so it is important that such love is sincere. Elephants have a rapid metabolism, and need regular feeding 24 hours a day, initially on
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demand; but gradually adapting to a three hourly feeding regime throughout the day and the night during their first fully milk-dependent year of life. From the age of five months the milk formula can be fortified with cooked oatmeal and desiccated coconut. The calf should also be offered natural browse hung in the night stable, but the browse will only become important during the second year of life, which is also milk-dependent, but is a gradual weaning-off-milk stage as the calf s intake of vegetation increases. Baby elephants can be weaned off milk after their second birthday, but will need supplementation with coconut, which contains the correct type of fat, for another three years, and even beyond during extremely dry periods. Our youngsters growing up in Tsavo are supplemented with Copra (the waste of coconut) and boiled barley once a day when they return to their night stockade in the evenings. If the orphaned Nursery elephants are doing well when they reach the age of one year, they are transferred to Tsavo National Park to be absorbed into the older echelon of orphans, and to begin their weaning year and long and gradual period of reintegration back into the wild community. It must be understood that at any age an elephant duplicates its human counterpart in terms of age progression and development. For two years an elephant can be classified as an infant; as a child until the age of 10; a teenager between l0 and 20 years, a young adult in its 20s; mature in its 30s and 40s, and becoming elderly by the age of 50. Their longevity mimics humans as well, influenced by factors such as stress, diet, clean air and water; however, given protection and favorable circumstances, an elephant should normally live into its 70s and even 80s, as do humans. Our orphaned elephants are usually not ready to leave the care of the human family until they are around the age of 10. This depends upon the age at which the baby elephant was orphaned. Those orphaned in early infancy (i.e. younger than one month of age) will have no comprehension of their lost elephant family. Those orphaned when older will always remember their time within the herd, and usually make the transition earlier than those orphaned very young. Elephants communicate with a spoken language that they need to learn from other elephants, and a body language that is instinctive at birth. The younger the orphans can be exposed to older elephants, the easier will be the learning and transition back into the wild system. Furthermore, acceptable behavior must be taught, initially by the human family during the Nursery period, then by the older, still dependent orphans in Tsavo and then ultimately by the wild community. Elephants are born with knowledge important to survival as well as a genetic memory, both of which can be honed only by exposure to a wild situation. All these factors are reasons to return the infant elephants to a wild situation as young as possible, and to complete the second milk-dependent weaning year amongst older elephants, with exposure to the wild community. In Kenya, the Nursery elephants are transferred to Tsavo East National Park, which is Kenyas largest Protected Area, 8,000 square miles in extent. This park holds Kenyas largest single population of elephants, currently numbering some 11,000. The reintegration process Elephants are highly social animals, and all elephants are drawn to the young. Consequently they are one of the easiest species to return to the wild, providing the wild herds have not been severely harassed and traumatized by humanswhen, for instance, human scent on an orphan might trigger antagonismand also providing the calf is normal psychologically. The older orphans in Tsavo always welcome any newcomers, and escort the youngsters into wild herds already known to them in their daily wanderings. The length of time it will take for an orphaned elephant to become a wild elephant,
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comfortable within, and a member of, the wild community is, however, influenced by various factors: 1. At what age the elephant was orphaned, and how well it can recollect its elephant family and other elephants. 2. The personality of each individual, just as with us humans, differs. Some elephants are outgoing, independent and adventurous; others are timid, shy and retiringmore dependent on their human family. 3. Friends, i.e., an orphans other orphaned elephant friends. Just like human children, elephants are more comfortable when they can count on the backing of their friends during exposure to the unknown. Those that have been raised alone in the Nursery without the company of other orphans feel more vulnerable and insecure than those who are bonded by friendship and can travel as a group. Each orphan decides when to leave the human family and become a wild elephant again. The choice of when rests with each and every individual and usually depends upon their having befriended wild calves of their age. They are never tipped out, as suchjust introduced gradually through access and exposure. Once wild, many still keep in touch, returning when and if they choose, to visit their human and orphaned family, or when in need of assistance. An elephant never forgets, and each orphan will remember and love those particular individuals who comprised its human family during infancy and adolescence. This love does not extend to all humansit encompasses only specific individuals who represented the family, and who will be recognized immediately years later. An instance is when Eleanor, aged 42, immediately recognized, after an absence of 37 years, the keeper who cared for her when she was five years old. The cows All female elephants long to nurture and love those younger and smaller. Female elephants are naturally maternal, a feature that manifests itself in the Nursery, with older female babies caring for and protective of those younger. Female elephants all long for a family, and orphans who have lost their natural family and who grow up as self-appointed matriarchs often resort to trying to snatch young babies from the wild units, something that is not popular with the wild matriarchs and breeds dissension and resentment within elephant society which, in a perfect world where families are intact for life, should not exist. For us, the ultimate destiny of the large group of orphaned female elephants that are still with us remains an unknown learning curve, because never before has anyone had to cope with so many young elephants under the care of older self-appointed matriarchs, with juniors taking on the role of nannies. Matriarchs and nannies are responsible for the well-being and safety of the herd. They keep the peace, instill discipline in the unruly and opt to care for any young newcomers. Previously, the orphaned females that survived during the 50s, 60s and early 70s were all orphaned much older than two years of age, and, remembering their elephant families clearly, became absorbed into wild units while still young. The current situation in Tsavo is unique, comprised as it is of elephants orphaned as newborns or in early infancy, so the attachment to the human family is stronger and very different to earlier times. I am confident that the female orphans will remain together as a herd into adulthood, always caring for the youngsters who are transferred from the Nursery and keeping in touch with those that are still accompanied by their human family, and yet to make the transition. The erstwhile young matriarch named Emily, who is now free amongst the wild community, along with her nannies and another young female, still keeps in touch with the dependent
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orphans, and assumes the role of matriarch to them whenever she returns. When she peels off to go her own way again, the next oldest automatically takes over leadership of the orphaned group. Those humans who represent the elephant family are greeted with the same love and affection that Emily, Aitong and Sweet Sally offer to their extended elephant family of orphans. The bulls Just as human boys and girls are different, so are the bull and cow elephants. The young bulls are more independent and more competitive within their peer group, and are always eager to dominate and become top dog, a position that others constantly and continually challenge. Young bulls wrestle a lot and tend to be much rougher in play than their female counterparts. They tend also to be more unruly, more mischievous and adventurous and sometimes more badly behaved, deriving apparent pride out of generating admiration from their peers for exploits that cross the boundaries of acceptable behavior. It is very normal for young bulls to develop a kind of hero worship for the dominant males within their society, emulating their example and learning from them what elephants need to know to limit conflict, for elephants fight seriously only when evenly matched in age, rank and tusk size; such encounters can often end fatally for one or both parties. It is important, therefore, for a bull elephant to know his place within the male hierarchy, a learning process honed whilst growing up and being exposed to the wild elephant community. It is also not unusual for young bulls to suffer from a feeling of inferiority if they happen to be of a more submissive nature and cannot dominate their age mates. This will also become evident if they have had a rough time from wild age mates as well. During this phase, they tend to throw their weight around among those that they are able to dominate, i.e. the younger elephants and the human keepers. An example of this is a teenage bull, Imenti, orphaned the day he was born. Having never suckled his mother, he was deprived of the first colostrum milk and developed a defective immune system. An infusion of blood plasma taken from an older elephant saved his life, and since then the Trust has been able to successfully hand rear another such immune-deficient candidate. Imenti shared his Nursery year with our young matriarch, Emily, of whom he is extremely fond. In Tsavo he grew up amongst other young bulls, all of whom were older and more dominant, so it is Emily with whom he is most comfortable, assigning himself the role of guardian, for instance chasing off buffalo and other intruders he views as a threat to the younger orphans. He grew to the age when he was not welcomed into the female wild units by wild matriarchs, and when he should have been seeking the company of other bulls, but his deep love of Emily retarded this step. Within the orphan group he was a big fish in a little pondout in the wild with other bulls he was a little fish in a big pond. His behavior during this phase of his development can be likened to any human teenager, with the same set of hang-ups, and in the end he was translocated to the northern area of Tsavo East National Park, where after a year of human dependency, he has finally made a successful transition. Imenti now lives as a perfectly normal wild elephant, shunning human company, as does the entire wild elephant community of that area, which has been subjected to three decades of rampant poaching for ivory in the late 70s, 80s and early 90s. Elephants can communicate a sophisticated message to one another, and Imenti has received this message from his wild peers, loud and clear. The solution The orphaned elephants raised in Kenya are not trained to do anything they would not
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normally and naturally do, except during their initial Nursery year when they are taught not to knock down human onlookers, through tone of voice by their keepers and the waggling of a finger. When a young bull becomes a teenager, he must be respected as would a wild elephant bull. There must be no attempt made by human attendants to dominate him in any way, and to prevent him from going wherever he wishes (see Chapters 14 and 15 by Buckley and Derby). This will only result in resentment and exacerbate the situation. He must be ignored completely by both the keepers, and all human onlookers, who must, at all times keep a safe, limited distance, as they would were he a totally wild elephant. If he charges a moving vehicle, the vehicle must get out of the way, as it would were the elephant wild. In a national park, animals have right of way and humans are mere visitors and onlookers. All tour drivers should understand this, because elephants can be dangerous and must be given space. It is never a good idea to place oneself in a compromising position where escape is impossible. The aim of our Orphans Project is to rear the orphaned elephants in such a way that they grow up psychologically sound so that in the fullness of time they can be returned to where they rightly belong, amongst the wild elephant community of Tsavo National Park, there to enjoy the quality of life as wild elephants that is their birthright. Once elephants are fully rehabilitated and living amongst the wild community, it is important for humans to understand that an elephant that once trusted and loved humans may not be quite as accommodating after having been told about the experiences of others at the hands of humans. It is always wise, therefore, to allow a returning adult ex-orphan to make the first approach, for he or she may not want very close contact, even with the humans that replaced its elephant family in infancy. As of June 2008, the David Sheldrick Wildlife Trust has successfully hand reared from early infancy over 85 orphaned African elephant calves, eight of whom are still in the Nairobi Nursery, 30 still dependent but growing up in Tsavo East National Park in the process of rehabilitation, and 36 now fully rehabilitated and living normal wild elephant lives, separating on occasion into two separate units, and on other occasions traveling as a bonded herd. One of our young cows died giving birth at the age of 10, surrounded by a grieving human and elephant family, amongst those she trusted and most loved. After 10 days of grueling labor, she had to be euthanized humanely, as the unusually large calf, which had died during labor, was lying breach, blocking the birth canal. The others are now fully independent and reintegrated back into the wild community; some of the females have borne young in the wild, and brought their calves back to be introduced to the other orphans and the erstwhile human family. In conclusion, I can vouch for the fact that elephants possess all of the best attributes of the human animal, and few if any of the bad. Despite their strength and size, they are essentially gentle, caring and kind, coexisting peacefully with all other creatures that share their world. In this respect they can teach us humans a great deal. It has been a privilege and an honor to have been able to atone for the cruelty of humankind in a small way.

Dr. Dame Daphne Sheldrick, DBE, MBE, MBS, DVMS is the Chairperson of the David Sheldrick Wildlife Trust. She has operated the Orphaned Elephant Project for 20 years.Dr. Dame Daphne Sheldrick was recognized as the 1992 UNEP Global 500 Laureate.She was also winner in 2001 of the BBC Lifetime Achievement Award. She may be contacted at The David Sheldrick Wildlife Trust, PO Box 15555, Mbagathi 00503, Nairobi, Kenya or rc-h@africaonline.co.ke.
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Paul F. Waldau The New Visions in these two papers have been shaped as the authors engage two important conflicts in modern captivity. First, each author confronts the inevitable tension between, on the one hand, existing practices, facilities and assumptions in modern industrial societies regarding captive elephants and, on the other hand, guidelines that flow from each authors commitment to a science-informed, ethically sensitive vision of these animals as beings valuable and worthy in and of themselves. The authors also negotiate a second conflict, namely, the tension between limits imposed by practicality and the parameters of their visionary guidelines. It is these tensions that push our society in pursuit of a meaningful human-elephant relationship, and thus warrant close attention. These conflicts and tensions are undeniably realin combination they are described in Hancockss essay as the tattered tail of tradition that wags the future of zoo development. Williamson, after arguing that our exhibits fail precisely because we are far more focused on economic considerations than upon the needsthe health, welfare and, ultimately, the survivalof elephants and other species we claim to love and care for, suggests what it will take to do justice to their uniqueness as a species. Whether these insightful pieces do in fact describe a future scenario that is achievable and that could make the accommodation of elephants in zoos acceptable and of value (Hancocks) can and should be debated. What is clear now, however, is that new visions for zoos must engage in detail, as Williamson and Hancocks aspire to do, these challenging problems. The very act of trying to see the future will influence in both obvious and subtle ways our societys ability to move toward a human-elephant relationship that is a celebration of elephants abilities, and ours.

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Chapter 17 What Will New Zoo Environments Look Like?


David Hancocks, M.Arch. When asked to address this question, I realized that my ability to predict the future enjoys a track record about as useless as that of professional astrologers or clairvoyants. Therefore, instead of attempting to describe what new zoo environments for elephants will look like, I have described what they could be like. Here is a future scenario that is achievable and that could make the accommodation of elephants in zoos acceptable and of value. The proposed size of spaces and number of elephants in this scenario are what I consider an acceptable minimum, but they are not an optimum. Indeed, if the tattered tail of tradition was not so determinedly wagging the future of zoo development, I would propose that there should be no new zoo environments for elephants unless they matched the standards set by the sanctuaries in California and Tennessee. If zoos were today approaching the question of elephants as a new problem, without being hampered or misdirected by historical precedents, more of them would surely recognize that elephants are not good candidates for their collections. In reality, however, zoos will continue to display mega-vertebrates. The fierce resistance of so many zoos, circuses and aquariums to part with large animals, even ones they keep in degrading circumstances, makes it clear that they will insist on keeping the biggest ones of all. Let us then consider what could make the experience of seeing elephants in an urban zoo worthwhile, perhaps even wonderful. I have constructed a scenario set in early spring in the year 2020, a year of clearer vision than our present one. On this day we are accompanying a family visiting an American zoo that has transformed itself with a remarkable new exhibit for elephants. This zoo is situated in a part of the country where average temperatures typically do not fall below 40 degrees Fahrenheit (five degrees Celsius) or rise above 90 degrees Fahrenheit (32 degrees Celsius) for prolonged periods, because in recent years professionally operated zoos have agreed not to keep elephants in climates that require lengthy periods indoors, or that adversely affect the animals comfort to any notable degree. Unusually, the zoo we are visiting is in an urban area. Most zoo visitors wishing to see elephants in 2020 tend to head out of town to open-range zoos. The space requirements for elephants are now much more liberal, and the days of 1,800 square feet as the official zoo standard for outdoor space for an elephant, with half that amount for indoor space, already seem like something from the Dark Ages. Furthermore, urban zoos in 2020 typically focus their attention upon interpreting ecological displays, and emphasize small life forms rather than the assemblage of big mammals that dominated city zoo collections in the 19th and 20th centuries. Following disastrous weather patterns from pollution-induced global warming, and the continuation of massive losses of biodiversity, communities have become more environmentally aware. As a result, many urban zoos have responded by concentrating on broader environmental stories, such that, in 2020, they now look and feel more like animated museums, and act more like proactive environmental and wildlife resource centers for their local communities rather than just a warehouse of creatures on display. The few zoos exhibiting elephants in America are now located on sites where they can offer
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much larger spaces than were ever contemplated in the previous century and can maintain much larger herds. The days when zoos unabashedly talked about a zoo herd of two elephants, such as Seattles Woodland Park Zoo (WPZ Press Release 2006), are now recognized as merely self-serving and preposterous. Many of the new elephant enclosures are so large that visitors tour them in safari vehicles and often stay overnight to immerse themselves more thoroughly in the experience. It is all very different from the typical two-hour tour with hot dogs and popcorn that characterized zoo visits of the recent past. Having initially rejected the standards set by Americas first elephant sanctuaries, in California and Tennessee (e.g., Hutchins 2004), the American Zoo and Aquarium Association (AZA) now models many of its regulations on those sanctuaries philosophies and operating policies. The zoo we are visiting today cannot achieve such huge spaces for elephants on its urban site, but it has devoted more than 20 acres (eight hectares)almost one-third of its total groundsto them, and presently has a group of seven elephants. The increasing rarity and iconic status of elephants encouraged this zoo to make considerable investment in its elephant exhibit. It then capitalized on this substantial dedication of land and finances by planning its entire layout and its collection around elephants and their habitats. Everything the visitors see and experience is now a part of or in support of the elephant story. This approach has helped to guarantee both the complexity and the value of the visitor experience. The high quality of this experience in turn ensured high levels of visitation. Increased attendance then contributed to wild elephant research and habitat conservation, for our zoo has signed up to the One Percent for Conservation program introduced by the newly emergent liberal faction of the AZA. In this program a member zoo pledges one percent of its operating budget to its Wildlife Conservation Fund. Concurrently, the AZA has also introduced two other useful conservation programs: one is called Sharing Our Common Knowledge, or SHOCK, and the other is called Adopting Wild Environments, with the acronym AWE. These new American programs, SHOCK and AWE, require every member zoo to align formally with one specific wild habitat and to share its economic and intellectual resources with people working and living in the region of that habitat so as to assist with its survival and wellbeing. Each zoo commits to share not only its own captive husbandry information and research, but also to encourage and facilitate appropriate knowledge from professional and academic sources within its own community. Thus an army of American teachers, politicians, lawyers, educators, doctors, planners, veterinarians and other specialists are now cooperating with their local zoos to help protect and improve selected wild habitats around the world. Specific subsets of the AWE program have also emerged, to assist particular species or habitat types. One of theseAdopting Wild Environments to Save Our Mega-vertebrates from Extinction, or AWESOMEencourages each zoo to formally adopt one specific wild habitat location that supports big animals, and especially elephants. In this program each zoo maintains direct contact with its chosen habitat locality, such as arranging tourist visits, sending staff members and other specialists to provide assistance, and fundraising from within the zoos membership base and its business community. It is why the zoo we are visiting this morning is asking its visitors and members to vote from a selection of wild elephant research programs for funding adoption. Through such programs Americas zoos are bringing direct contact and knowledge of specific wild places to the attention of their huge numbers of visitors. Initial research suggests that this enriches the sense of value zoo visitors gain from their attendancethey feel positive about the fact
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that their visit makes a difference, and they form a strong sense of allegiance to and partnership with the zoo in its habitat conservation efforts. At last, almost 200 years after the first modern public zoological garden opened its gates in Londons Regents Park in 1828, zoos in wealthy countries are beginning to serve as effective bridges between their visitors and the conservation of wild places. In this second decade of the 21st century, zoos are serving as links between their two conflicting major clientshuman audiences from urban environments, and wild animals from wilderness habitatsboth metaphorically and in practical ways. They have finally graduated to a position where their existence is justified, their philosophy is meaningful and their purpose is truly valuable. The tour begins Our zoo visitors leave their hydrogen-fuel-cell vehicle in a tree-shaded parking lot of permeable pavement. One section is reserved for stackable and shareable all-wheel robotic inner-city vehicles. Water-retentive planting swales around the parking lot ensure zero discharge of rainwater. This facility is just the first example of many sustainable construction techniques employed throughout the zoo. Zoos have been claiming to be Conservation Centers since the 1980s, but only in recent years have they recognized all the accountabilities accompanying that status. Our zoo has adopted those responsibilities enthusiastically. At the side of the parking lot are passenger vehicles just 10 years old but now universally regarded as dinosaurs, including a Dodge Ram, a Ford Excursion and a Hummer, with a graphic panel showing the combined impact such American automobiles had on atmospheric pollution, global warming and habitat loss. This side-bar exhibit is an indication that this zoo has important things to say. In fact, the zoo visit has already begun, here in the parking lot. There is no visible fence to declare the perimeter of the zoo site; instead, visitors enter a garden area, a botanical sanctuary that acts as a buffer between the outside world and the zoo proper. This restful garden landscape acts as a decompression zone. There are no lurid colors and animal logos here. It is instead an invitation to slow down, to enter a world that rewards careful observation. The garden gives visitors time to unwind and to reorient. A volunteer greeter reinforces the sense of welcome and offers maps, advice and general guidance. The garden pathways lead visitors to a building with an entryway that, through attention to design and detail, underscores a notion of its importance, rather like a successful museum or art gallery. Inside, in a quietly appealing but visually rich environment, are exhibits dedicated to all aspects of African savannas, but with a special focus on elephants: their life histories, habitats, evolution and their historical and present-day threats. We learn of elephants behavioral biology, of the intricate nexus of interactions with their diverse natural habitats. We learn to see anew this huge terrestrial animal, whose size both confers physical capabilities and imposes limitations that have influenced social structure, nutrition and foraging, communication, courtship, mating, infant development and care, emotional perception and intelligence. The ecological roles of elephants and their interdependence with other creaturesfrom dung beetles and tick birds to baboons and lionsis also examined as part of this holistic presentation on the planets largest remaining land animal. Recent knowledge of wild elephants is discussed via live audiovisual links to research activities in the wild. Throughout the hall are films about elephant life, shown on screens from jumbo size to personal computers. Dioramas display models of elephant herds and other savanna animals in miniature habitat displays of superb veracity. Lifesize models show living and extinct species.
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Touchable artifacts such as bones and fossils, sound booths that reveal the complex acoustical world that elephants inhabit, and all manner of other devices and interactive media uncover the diverse stories of modern elephants and their amazing relatives, both small and massive, that in such recent times walked the earth. The wonder as well as the fragility of the continuing existence of elephants in both Asia and Africa is made plain. Emerging from the interpretive hall, our visiting group starts a journey into a replicated wilderness habitat that looks, feels, even smells and sounds like African elephant savanna country. This landscape has been designed to create the impression of an exotic land: meticulous attention has been devoted to emphasizing in exquisite detail the parts of the habitat that reinforce that view, and to eliminating the pieces that degrade that sensation. The place feels nothing like the cluttered pastiche of the traditional zoo with its mlange of animal exhibits. The landscape here is not merely a background that one blindly travels through to get from one exhibit to another. Neither does it carry the usual zoo atmosphere of a suburban park sheltering exotic intruders. All the accoutrements that generate such characteristically bizarre impressions have been studiously rejected. Thus there are no merry-go-rounds, no flower beds, no acres of asphalt and miles of fencing. Nor is there a Rainforest Caf selling hamburgers and fries. There are no signposts with arrows to gorillas or tigers, or, indeed, any signage of any kind. Instead, as the visitors follow an interwoven pattern of meandering red-earth paths, the forested tree canopy fragments into thorn-bush and savanna scrub habitat. Views are opening and closing as the visitors walk past truck-sized ant-hills or termite mounds reaching above head height, and maneuver through swales or enter thickets of grasses that grow taller than they can reach. A cluster of palm trees grows near a wide shallow river, beyond which are the distinctive building shapes of an African village, surrounded by indigenous crops and accessed by a rickety bridge. This replicated village (Figure 1) mirrors the vernacular architecture of a specific locale. It is not treated as some ersatz oddity that provides only a transitory backdrop for a sales pitch of beads, t-shirts and ice cream. Instead it serves as a stage for interpreting both cultural and natural history,

Figure 1. Visitors encounter an authentically replicated African village in a naturalistic landscape. 218

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revealing, with respectfulness, the ways in which this particular settlement and its culture have developed in response to a particular landscape and natural environment. It is why the customs, music, beliefs and stories presented in this village are unique. The administrators of the zoo we are visiting today recognize that the idea of captive animals as effective ambassadors for their wild cousins is more than a mere promotion ploy. They have set out to ensure that the entire volume of experiences for visitors reinforces and supports this notion. This is why they have given such close attention to the context within which they present their elephantsa context that is culturally and ecologically authentic. Their reasoning is that simply displaying elephants is insufficient, and cannot achieve any of the goals of ambassadorship; wild animals such as elephants cannot be understood unless they are presented and explained within the natural environment in which they evolved, and in relation to human society in their home ranges. Similarly, this zoo has dedicated much careful thought to whether they should have elephants, and to the purposes that could justify their ownership of them. Initially, the administrators had to battle with board members who regarded the question as absurd and considered the inclusion of an elephant in the zoo as a normal and even essential ingredient of the collection. One influential donor asked, How can you call this place a zoo if you dont have an elephant? Fortunately, he had a teenage granddaughter who was able to dissuade him from that type of thinking. Another board member grumbled about the new AZA requirement for a minimum number of five elephants but grudgingly accepted it as a necessity for accreditation. Some long-time board members representing commerce and industry were especially reluctant to consider anything other than quantitative data, and were suspicious of any assessments based upon qualitative criteria. They were much more comfortable trying to manage rather than to solve a problem or attempting to establish a new paradigm. But this type of thinking in 2020 is increasingly in the minority. The collapse of the one-size-fits-all mentality of globalist ideology, coupled with an almost universal realization that many technological solutions were only short-term band-aids, has ushered in a generally new way of thinking, a recognition of the needs for cooperation, and the importance of local values. Now, in 2020, more people seek to become board members of local cultural institutions such as zoos because they believe these places should make a difference to and enrich the values of their own communities. Board membership is no longer typically pursued simply for status, or for making useful social connections, or to look good on a business rsum. In addition, thankfully, a national accreditation system now scrutinizes boards of cultural nonprofit institutions, requiring them to focus on governance and not to act as managers. This has unleashed enormous freedom for creativity among administrators, as well as enabling them to hold a conscientious dialog with their wider community about the role and purpose of the zoo. These changes have also accompanied shifts in general public attitudes towards funding levels for education, and towards environmental health and welfare, and are now manifested in myriad ways, including revolutionary adjustments in communal views about keeping elephants and other animals in zoos and circuses. There had nevertheless been much relief among zoo board members when a study revealed that a 20-acre exhibit area for elephants was not necessarily 20 times more expensive than a oneacre exhibit, that the proposal for this bold move resonated very positively with a majority of those surveyed in focus groups, and that the drama and excitement of this new exhibit attracted attention nationwide. Not having to build updated exhibits for large animal display spaces that were being replaced
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by the new elephant site was also a welcome and substantial saving in costs. Surveys showed that deletion of many of these big animal species from the collection would not result in any loss of public interest if there were a concomitant broadening of the zoos vision. Indeed, the addition of a great variety of small (and sometimes very small) life forms had increased the level of interest for many visitors. The introduction of museum-type displays, and opportunities for interacting with several different media, also increased the average length of stay, with a subsequent increase in sales of refreshments and educational material. The zoo had closed while it rebuilt itself. It had also sensibly allowed an extra year beyond the projected completion date, not only to accommodate the inevitable delays but also to give the new plantings time to become established. Soft openings were celebrated as sections of the new zoo came on line. The tour Our family of visitors is making its second visit of the year to this zoo. They have discovered there is now too much to see and do in one visit. Nor is the journey they take today simply a repetition of their previous visit. The pathway system around the site has been designed in a series of closed loops to insure that people do not get lost. Thus, visitors never encounter a choice between two or more paths. They can devise a different route of exploration on each visit, without concern that they might inadvertently not get to see one section or another. Every detail of the journey is designed to reflect the sense of adventure and discovery that comes with a walk in a wild habitat, and each journey ensures a new sequence of experiences. There are no signs directing them to specific exhibits, and the map marks only the outlines of various types of habitats and the trails that can be followed to explore them. As with a wilderness experience, what the visitors find within those habitats is not predictable. In this zoo the landscape (Figure 2) is not just a background to be walked through on the way to a predetermined animal location. The landscape is the zoo, and the animal encounters within that setting acquire much greater value because of that. The site has a mosaic of many different types

Figure 2. The zoo landscape is designed to create a sense of adventure and discovery 220

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Figure 3. Massive granite outcrops sometimes break on to the scene.

of African savanna habitat, from forested woodland and thorn-scrub to open grassland and swamp. There are acacia and mopane thickets, areas that look almost park-like, as well as shrublands and bushlands, broad open grasslands, and densely vegetated riverine environments. In particular there is much variety in tree cover and a surprising diversity of shrubs and grasses. Interactions with very knowledgeable and rigorously trained volunteer rangers at stations along the way expose the visitors to information about many and diverse aspects of these landscapes. Visitors can thus tailor their exploration to suit their own wants and needs. Visitors occasionally encounter animals in their travels through the various habitats. These generally mirror the composition of species found in the wild savannas. Thus there are herbivores and predators, small animals such as rock hyrax, mongoose and caracal, a large colony of active vervet monkeys, several species of reptiles, amphibians and many invertebrates. Large birds fly in vast, almost invisible enclosures, where weaverbirds create masses of their very visible nests. In one location a baboon colony makes a spectacular and active display. In another, the experience is more serene as visitors watch waterfowl patiently patrol a wide shallow swamp. The variety of encounters is orchestrated to create diverse moods and varying levels of excitement or relaxation. Not just animals, but a wide span (Figure 3) of African savanna ecology and geology is illustrated and interpreted by the volunteer rangers. Their personal interaction with visitors allows them to judge varying levels of interest and awareness, so that each presentation is different in tone and depth for each visitor. This method of interpretation also means that the replicated wild landscape is not littered with graphic panels, those expensive and intrusive interpretive elements that most visitors patently do not gainfully read.
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Some of the ranger stations are simple canvas shelters, like open tents, or are placed in the shade of a large spreading tree. Other stations are slightly more substantial, modeled on appropriate African architectural forms and materials; these larger stations include a composting toilet, provide opportunity for simple refreshments and offer guidebooks, sunscreen or other essentials for sale. Many of the ranger stations have benches or canvas chairs, and there is usually a table for close study of artifacts that the rangers have in their kits. One of the stations is beside a shallow stream where kids can paddle or play in the mud. Another is next to a pool where children collect aquatic bugs and other pond life in jars for close examination. A station that provides fair-trade East African coffee is adjacent to a huge pile of granite rocks that are a natural play area for kids to clamber over and explore. The rangers also act as guides, and recommend general directions towards places where visitors might increase their chances of seeing a particular species of animal. It is rather like a safari in Africa where a chance encounter with someone who has good local knowledge gives an insight into the complexity of the habitat, and from whom one might learn that a leopard has been spotted in a thorn tree beyond the horizon, or a family of warthogs is likely to be seen in a nearby wallow. Elephant viewing Although the pathways meander via the several closed-loop trails through a variety of different habitat types, they all eventually lead visitors to the area in the zoo where the elephants live. The pathways around this part of the site take people to different elephant-viewing areas. Each of these lookout points, however, is difficult to recognize as a designated viewpoint. Barriers carefully mimic natural features, so no sense of enclosure or separation is apparent. The viewing areas look remarkably like any other section of the path. Thus, when elephants are seen, it generates the same rush of excitement that occurs when discovering an animal in the wild. The 20-acre area for the elephants enclosure is designed in such a way that the whole of it cannot be viewed from any one spot. This avoids any sense of enclosure. Viewing locations vary; some are discreet and secluded, others are open and expansive. Sometimes views are glimpsed only through copses of trees, or are partially obscured by scrub plantings. The viewing sites have been designed to create a series of unfolding views and changing discoveries that heighten the theatrical effect of the whole encounter. In places the path leads away from the elephants exhibition habitat, but because there is no perception of any means of enclosure, this departure is never evident to the visitors. Instead of merely observing from designated viewing points, visitors gain and lose sight of the elephants as landscape features open or conceal views. Moreover, the landscape in adjacent public and animal areas is identical, and barriers are disguised as natural features such as streams, fallen trees, grassed berms, land slippages, swampy mud and so on, and thus are never recognized as fences. Taking the path away from the elephant viewing experiences brings several advantages. It creates a heightened appreciation for the elephant experience when the views are returned; it gives visitors time to focus upon the vegetation and to simply absorb the beauty of the replicated landscape and the diversity of its features; and it allows the introduction of exhibit areas that display other animals. It reminds us that good exhibit design is like good art. Each is an artifice, and the sequence and selection of what is not seen is as important as what is revealed. The various views into the elephant area open onto sections of the enclosure that are each quite different. At times, distant panoramas reveal wide and open undulating grassy areas, and at other places the scene is only a glimpse into shaded smaller sectors, some narrow and enclosed by tall grasses or other dense plantings. Tall acacias and other broadly topped trees are scattered either
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as individual giants or in clusters, and they provide shade both for visitors and for animals. When elephants are seen they might be nearby or distant. They could also be indulging in a variety of activities: wallowing in a large mud hole, or in a cloud of dust at a sandy area; digging into an exposed cliff to get at salted minerals; fording a wide shallow river; lying down for a rest on a grassy bank; climbing up steep slopes; clambering over large rocks; or splashing and cavorting in a series of small pools. They are not, like so many zoo elephants used to be, controlled and activated by a dominant zookeeper. The views that visitors enjoy are not always at eye level. In places the path dips and the elephant area rises, so that the massive size of the animals is exaggerated. They are then seen well above ones head, silhouetted against the sky or a backdrop of tall trees. Indeed, the topography of the entire area is markedly divergent and ever-changing. There are locations, too, where visitors might find elephants breaking what appear to be live boughs from a tree, stripping the bark and cracking the limbs. A particularly well-favored viewing place is located at one of the low spots along a pathway, in front of a swamp, where the elephants especially enjoy spending time on late summer afternoons gently foraging among plants growing in the shallow waters. A ranger station at this location provides opportunities for visitors to converse with volunteer guides while resting awhile, making use of loaned binoculars and guidebooks on savanna ecology, and enjoying the simple refreshments that are offered at this spot. In some places along the path, smooth and large rocks provide opportunities to pause, rest and enjoy the scene, or a fallen tree affords a surprisingly comfortable bench for a perfect viewing spot. Youngsters in particular love one of the viewing locations that is approached by crossing a small stream via stepping-stones or, for the more adventurous, a large fallen tree. Sitting by a stream that gurgles and splashes over smooth river rocks, in the dappled light of a lushly grassed embankment, visitors are encouraged to observe the elephants and their environment in a slow and observant frame of mind. The finale Turning from this scene, the path rounds a hill and uncovers a view of the stream plunging over a cliffside into a deep pool. Here, characterized by palm-like dracaena and an ancient fig tree, a shady entrance leads visitors into a lava tube cave. Such caves are formed when molten lava flows down a slope and the outer layers cool and solidify while the inner core continues to flow, leaving behind a tube formation. The cave is cool, lit by shafts of light from holes that have collapsed in the ceiling. It is a place of intrigue and wonder. The tube formation, easily large enough for our family to walk in, leads downwards and opens into a large exhibition hall that has the feel of a museum interior. Here the zoo showcases the story of deep time. A box containing one bright little dot the size of a pinhead explains that if this were the actual size of our sun, the next nearest starapproximately that same sizewould be located almost two miles away. Another exhibit allows visitors to touch a piece of moon rock, and, more amazing, a rock that originated outside our galaxy and is more ancient than Earth. There are interactive exhibits on topics such as volcanic forces, plate tectonics, and, of course, on evolution and the long periods of time required for its processes. One of the evolution exhibits explains how eyes evolved, and compares different ways of seeing and sensing the world among mammals, birds, reptiles, invertebrates, amphibians and fish. Other exhibits tell the story and the probable causes of the major extinction phases that our
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planet has experienced, and highlight facts about the one that is currently underway. An exhibit on elephant evolution reveals the remarkable diversity of the many elephantine species that have roamed the earth, some in astonishingly recent times, and outlines the human impacts on the survival of the existing elephant species. Exiting this exhibition hall, visitors move from an intellectually absorbing experience into a space dedicated to a purely sensory experience. It is softly lit, filled with gentle ambient music, and fronted with a view that resembles a gigantic aquarium exhibit with a floor-to-ceiling wall of glass. It exposes underwater views into a deep pool where elephants swim completely submerged, snorkeling in clear waters. Also seen here are many different types of colorful cichlids and other aquatic life of the area, from frogs and snakes to turtles and crocodiles, and several species of water birds. Like the kelp forest tank at the Monterey Bay Aquarium, this room, with its astounding views of elephants underwater, has become revered as an icon of zoo exhibit experiences. When people leave this magical place, they exit via a path that ramps up into a room resembling a juice bar cum coffee shop cum specialist library. Sofas and armchairs face a large window into the shallower reaches of the pools, which the elephants share with herons, storks and pelicans. It is a wonderful place to relax, to ponder, to be amazed and delighted, and, like a patio lounge at a safari lodge, it provides a perfect climax to the days visit. Reflections Walking back through the savanna landscape our visitors decide that on their next visit they will stay overnight, sleeping over at one of the three tented camps on the site, enjoying dinner, stargazing while listening to stories about African folklore and wildlife, participating in African drumming workshops around a campfire, and taking guided tours to explore the nocturnal activities of the elephants and their other savanna compatriots in this new and unusual zoo. On their diurnal visit, our visitors have been immersed in a medley of emotional, sensory and intellectual experiences. They have absorbed much information about all aspects of the African savannas: the geology, the plants and the animals, the cultural history, all in ecological and historical contexts. It has been akin to a concentration of the experiences one could encounter during a period of several days exploring a real elephant wilderness habitat. Our visitors have had their eyes and their minds opened to a deeper understanding of the world of elephants and of the world of nature. All this happened because this zoo was not content with merely putting elephants on display to show just their size and form, and did not attempt to arrogantly claim that zoos could solve all the difficulties for elephants and save them from extinction simply by exhibiting them and trying to breed babies. Instead, this visit has exposed our visitors to many new questions and to many unanswered problems. In 1961 a new American president laid out a memorable challenge, exhorting Americans not to ask what their country could do for them, but what they could do for their country. It would be a wise metaphor for zoos, which should stop asking what elephants can do for their attendance statistics, for their professional prestige, for their acquisitive stature. Instead, they must learn to rephrase the question, like the zoo we have visited this afternoon has done, and to ask what they can do for all elephants.

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References

Hutchins M. 2004. Whats in a name? Zoo vs. sanctuary. AZA Communiqu. August, 54-56. Woodland Park Zoo Press Release June 12 2006. Elephant bamboo returns to Woodland Park Zoo. http://www.zoo.org/pressroom/pr/2006/pr06_12_2006.htm

David Hancocks is an architect who received his B.Sc. and M.Arch. degrees from the University of Bath. He was director of Woodland Park Zoo (1976-1984), the Arizona-Sonora Desert Museum (19891997) and Werribee Open Range Zoo (1998-2003) and is a member of RIBA (the Royal Institute of British Architects). His latest book is, A Different Nature: The Paradoxical World of Zoos and Their Uncertain Future (2001), Berkeley, University of California Press. He may be contacted at 1 Queensberry Street, Carlton, Victoria 3053, Australia or at dhan8403@bigpond.net.au.

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Jeff Williamson President, Arizona Zoological Society As I write this, I am approaching my 33rd anniversary in the zoo business. During this time I have worked in the field, out on the grounds and in several administrative capacities. For the past 11 years I have been the director of a major urban zoo. All those years, I have taken part in daily conversations: in person, at conferences, through publications, over the phone and via email with many thoughtful people. Some were advocates, others were critics; some were within the industry and others were outsidersand the topics discussed covered nearly every imaginable area of our operations. From these conversations, I have learned a great deal not only about nuts-and-bolts matters but also about larger issues as well. I suppose it is only natural that at this stage of my career I am increasingly concerned with these larger issues. As I reflect on this time, both as a witness and as a participant, I am gratified by the progress we have made in some areas. Far more so, however, I am convinced that overall we have not done as well as we could have, that we are not doing well now, and that in too many cases we are headed in the wrong direction. My thesis is that we can and must do bettermuch, much better. How? First of all, we need to come to grips with some hard realities. There may be no better way to illustrate the issues than to look at how we deal with elephants, the species that we habitually and sometimes deprecatingly refer to as charismatic mega-vertebrates. * * * In my view elephant exhibits in urban zoosmy own includedare failures. This is not a mere matter of technology. No new, cunningly clever architectural designs will remedy it. Neither is it a matter of hardware or software or diet nor new techniques in veterinary care or keeper training. It is far more elemental than any of this. Elephant exhibits in urban zoos fail because they are woefully inadequate to the needs of the species. Elephants are intelligent, social and mobile creatures. We wrench them out of the wild in order to exploit them. We disrupt their herd structure and confine them in spaces that represent a tiny percentage of their daily range, then wonder why they develop chronic physical and behavioral problems: foot and leg trouble, arthritis, pacing, swaying and aggressiveness. Inadequate exhibits hurt the animals physically and emotionally. They do not get the amount or kind of physical exercise their bodies need. They do not have the sheer numbers of companions they need to form the communities in which to function as social creatures. We do not permit them space to escape occasional aggression from one another, a problem all the more acute in
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captivity where they often develop stereotypical behaviors verging on mental illness. In the meantime, we take pride in veterinary advances in the treatment of chronic foot and leg problems. As temporarily gratifying as these achievements may be to the people involved, they are merely band-aids from the elephants perspective. We are treating the symptoms but ignoring the cause: urban zoo exhibits deprive the animals of the opportunity to be what nature made them. We have debated exhibit size for decades now. The drift of these debates has been that X amount of acreage per animal is less than, adequate to, or greater than what the creature needs to live: and that if you alter things by Y, the animal will experience a quality of life change of Z, leading to a particular cost/benefit that will be judged according to the bottom line. There it isthe bottom line! The end point of all discussion. Our exhibits fail precisely because we are far more focused on economic considerations than upon the needsthe health, welfare, and ultimately the survivalof elephants and other species we claim to care for and love. With the elephants confined in deliberately inadequate enclosures, our interpretive programs are likewise doomed to failure. Just as we cut corners in housing the animals, similarly do we fail to do justice to their uniqueness as species, their adaptations to their natural habitats or to the critical roles they have played within natural systems throughout their evolutionary history. After decades of education programs, all too many of the schoolchildren and teachers we host regard a trip to the zoo as a mere break from the classroom routine. By the time they are 10, we have lost our children to the shopping mall and will not see them again for 15 years, when they bring their own babies to see the elephantfor a few years, that is. All in all, those children whether visiting with teachers or parentsfind it easy to forget about elephants, especially when they grow up and enter the shopping mallsand the voting booths. In fact, in education programs, we are especially hypocritical. Dissatisfied with static graphics based on data casually cribbed from encyclopedias and the Internet, we offer our audiences the chance to get up close and personal with our captives. We host behind-the-scenes tours during which we encourage visitors to give treats to animals that are already overfed and underexercised intellectually and physically. In doing so we demonstrateby our actions if not by our wordsthat the ultimate evolutionary purpose of these creatures is to perform obsequious gestures in exchange for industrial products of dubious nutritional value so people will think them cute and will buy more tickets. And, of course, at the same time we communicate that we zoo professionals are rightfully and properly the masters of such beasts. Again, the bottom line: we care more for revenue than we do for the health and welfare of the animalsor the appropriateness, honesty or integrity of the messages we send home with our audience. Naive visitors leave, not inspired, informed and eager to become advocates for wildlife; rather they leave confirmed in our societys prejudice that animals are merely resources, products and commoditiesparts of a planet for the taking, as David Suzuki pointedly said years ago. In spite of all we say publicly, what we demonstrate is something different: that elephants are merely large, bumbling, inept, rather temperamental and smelly caricatures of the human race and that we are justified in removing them from their natural habitats, depriving them of their liberty to be what the ages have made them to be, and dominating and exploiting them in any way we see fit.

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* * * By this point many readers will surely conclude that I am anti-zoo. Not so fast! Dismissing ideas out of hand is an ignoble strategy for ignoring them. If I am hostile to anything, it is to inadequate responses to urgent problems. Elephants and thousands of other species are in desperate trouble worldwide, in our zoos included, yet we fiddle away. My purpose, therefore, is to prompt a discussion that will lead us to face hard and uncomfortable questionsuncomfortable because we have tolerated a long tradition of neglect. Maybe, just maybe, such discussions will lead to badly needed improvementsfinally! Question 1: What is it that we are doing in zoosreally? Can we put aside the time-worn platitudes and face reality? If we cannot, I predict that the marketplace, global problems and the natural effects of inbreeding and disease, for example, will put an end to zoos far more efficiently and unsympathetically than I ever could. Question 2: Why are we doing itreally? Again, what lies behind the thousand veils of marketing, self-promotion and self-deception? Are we truly devoted to the creatures in our care? Are we committed to doing whatever is necessary to convince people to make life choices that respect nature? Question 3: Of what advantage to the elephants are our effortsreally? If our efforts do not benefit elephants, then they are biologically unsustainableand morally wrong. If only for a short while, can we leave behind our comfortable offices and unquestioned habits? Can we put aside the ankus? Can we leave the hydraulic controls for a bit, go over to the front of the elephant exhibit, and regard the animals sympathetically? Can we see them from the public viewing area, through the eyes of a small child seeing them for the first timeor are we grown too old and stiff and dull? What are the messages we are really communicating to such children, our successors, the decision-makers of the future? One way or anotherbecause of us or in spite of usthe children visiting our zoos today could grow up to love elephants and protect them in the future. But maybe they will go the other way, someday scarcely noticing when the news describes how, exactly, the last elephant in the world has died. Do we really think computer-generated holograms will thereafter be adequate substitutes? * * * We have all seen sepia-toned 19 -century photos from the earliest Western zoosLondon, Philadelphia and elsewhereshowing zoo directors and other dignitaries in top hats posing in front of iron-barred cages scarcely large enough for the inhabitants to turn around. In comparison, we feel inordinately smug today about the advances we have made since thenmarginal as they actually have been. Clearly, a reality check is in order: those iron bars were state-of-the-art back then. I submit that, despite our hubris, images of what we are so proud of today will look much the same a century from nowabout as quaint and out-of-date as the top hats. What I am asking then is whether or not we have the courage, imagination and fundamental decency to gonot to the clichd next levelbut way beyond that, to where we need to be instead? Can we make a quantum leapfar surpassing the distance from the iron bars to the zoo
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habitats and environments of today? Can we focus, once and for all, on the needs of elephants? To do so, we need first of all to reconsider our relationship with elephants, focusing on their well-being and recognizing that mankind has inextricably altered their world. Second, we need to reconsider the meaning of conservation and then, as a consequence, refocus our efforts. Third, we need to reconsider the urban zoo in the context of what is happening to the world environment and what will happen in the future. * * * In the first case, our relationship with elephants has nearly always been shameful and shortsighted. Rarely has it ever benefited them. To the contrary, we tolerate them as long as they benefit usif, that is, we can make them into a resource, a commodity. For centuries we have regarded the value of elephants mainly as beasts of burden. We find them usefulif they do work for usif we can eat themif we can use parts of their bodies as adornments or curiosif we can make them validate stories we like to tell ourselves about ourselves and our superiority to all of nature. In our own time, we find them interesting or delightful as charismatic mega-vertebrates, that is, big animals we can dominate. We allow their continued existence because we regard living creaturesand all too often our own kindas objects rightfully within our possession. Those things we do not find immediately usefulthings that do not lend themselves to our wants and needshave little hope of surviving in a world we are making increasingly crowded. Elephants are imperiled today precisely because our values are changing: our machines are supplanting their usefulness as draft animalsand, with our soaring populations, we covet the very habitats they need for survival. But what about elephants themselves? What about their needs? What about their right to existence? Do we ever consider needs other than our own? Can we? The basic question then is how can we help them survive in the futurerather than the other way around? * * * The second question regards conservation. Faced with a steady drumbeat of bad news about the outlook for wildlife, most in our industryas well as in academia and governmenthave responded in recent decades with the pious recitation of conservation. On its own, it is a fine, honorable term. Its general meaning is to protect, to guard, to ensure the survival of some asset elephants, for examplefor the future. More specifically, however, it points toward distinct responsibility, requiring that we humans restrain our appetites and our greed so that others may survive. Tragically, most of what we actually do in the name of conservation misses that point. In fact, in most professional usage, the word illustrates how profoundly we have mistaken the signpost for the destination. We have corrupted the term and deluded ourselves as a consequence. For the most part, we use it to mean to preserve species that are of value to us. Typically our conservation efforts are human-centered. They have more to do with our professional ambitionswith grants and larger staffs and new facilities, with databases or reports, with conference papers, advanced degrees, publicity, with new and better jobs and salariesthan they
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do with the welfare of other creatures, indeed of living systems. In our meetings and conferenceswhich, by the way, we attend in budget-devouring, carbon-generating, expense-account comfortwe talk of management as the key to success with our cherished conservation projects. Listen carefully, though, and you may hear something different. By management, we actually mean interfering with animals. We like to think of ourselves as virile, super action heroes. We like to chase animalsthe bigger the better. We like to herd them, dart them, install telemetry, move them, confine them and otherwise change their behavior. In other words we would find it more convenient if elephants would be something other than elephantsespecially in any place we happen to covet. Occasionally we cull them (notice the euphemism)for their own goodbecause our species has damaged their natural habitats to the point that they can no longer survive where and how millions of years of evolution have prepared them to live. When we thus manage wildlife, we are actually trying to dominate them, to bend them to our will. We are manipulating yet again the very creatures and living systems that are already victims of our thoughtless, intrusive, consumptive behavior. What we do not ever manage is our own thoughtless, intrusive, consumptive behavior. * * * The necessary corrective is to get back to the roots of conservation. We need to reconsider the way we, as people, states and nations, lead our lives. We need to face up to the consequences of the choices we as mass consumers make on what, how, where, when and to what degree we consume. What to consumewhat to conserve? We all want to think of ourselves as conservationistsbut how many of us are willing to change our goals and lifestyles to be conservationists? We all like to consume. We need to consume to stay alive. But how many of us are willing to change our patterns and quantities of consumptionso others can live as well? Can we live in ways that do less harm? Can we curb our own appetites, behaviors and egos so that elephants, and indeed all species, can survive these next ominous decades? In the future, management needs to mean managing ourselves. There is even a built-in, obvious appeal to our self-interest: can we restrain ourselves so that other species can live their lives, reproduce, survive and contribute to the health of the largescale systems everything, humans included, need in order to survive? * * * The third question asked about the future: Amid increasing concerns about overpopulation and global warming, what kind of world do we envision in the future? Will there be room for zoos? Vastly more important, will there be room for elephants? If the urban zoo is to survive, I submit that it can only do so by reinventing itself as something truly useful in the long run. It needs to become a place that serves wildlife and peoplelight years beyond the assurances of our four-color brochures. This cannot happen in urban zoos as we currently configure them. It cannot happen if we continue our current largely symbolic and ineffectual education and conservation gestures. It can happen if we live, perform and teach stewardship, if wenot just in words but in
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deedsadvocate and demonstrate good citizenship in the natural world. 1. Urban zoos need to craft compelling interpretive efforts to change the way people understand natureand, in doing so, initiate a change of course that will allow the survival of other creatures. 2. Urban zoos need to use our resources to establish rural refugia that foster the care and survival of elephants and other imperiled species. These two strategies must work hand in glove. Neither will work alone. Neither will work as long as we think of animals as curios and ourselves as the center of the universe, the top rung of the ladder of creation. To get to such a place, urban zoos need to shift their focus to demonstrating and advocating for stewardship. We need to engage our audience in protecting natural systems and cultivating values that support a reasonable quality of life for other creatures as well as ourselves. The urban zoo needs to evolve into a sharply focused center that would develop, train and export programs that inspire and build caregiving capacityin short, stewardship. The center would work with a regional emphasis on improving the health of the surrounding natural community. Its collections should be composed of animals either extirpated or physically unequipped to cope in a free-range environment, the social and physical needs of which could be met in a limited captive urban environment. The center would also breed populations for recoverythen develop skills in release, monitoring and restoration. Perhaps the greatest leap, however, would be that the zoo of the future would also establish and maintain rural refugia to support animals in need of sanctuary because their physical and social needs cannot be met in an urban environment. If elephants and similarly mobile species need more room, let us give them more room! * * * This is well within reach. Let me illustrate: Zoos do perform one important service fairly well: they allow us to provide protective custody. For the most part, we do make it harder for poachers to get to the animals than they can in the wild. The trouble is that we zoo leaders have not taken it seriously, choosing silliness instead. Periodically since the 1970s, we have enjoyed calling our institutions by such evocative titles as the stationary ark or the modern arkas if our confinements were something grand. But these terms were just words. The places they referred to were exactly the same un-Edenic collections of concrete, glass, steel and decorative landscaping that we have had all along. On top of that, we tragically undercut the value of protective custody if our exhibits themselves are harming the animals. But what would happen if we actually began living up to our wordsif we began walking our talk? What would happen if integrity broke out? With the global human population exceeding 6.3 billion, it is indeed well past time to get serious about providing protective custody. Opportunities exist now. With imagination and hard work we surely could find others. Public Law 1107-314 (Dec. 2, 2003), Department of Defense Authorization Bill, known as the Military Protection Act (MPA), provides one example: Amid the current population growth both stateside and abroad, military planners have
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Chapter 18 - Elephants in Captivity: Looking BackwardLooking Forward

recognized the need to preserve protection zones around military bases. Rapid encroachment of suburban and industrial development around installations raises the stakes dangerously in case of inevitable accidents and equipment failures. Essentially, protection zones are buffer areas intended to minimize hazards to surrounding population centers. Their value as safety and security measures directly relates to the scarcity of human presence therein. In recent years, conservationists in my state, Arizona, made a surprising discovery. When former and current bombing range lands were opened periodicallyor in one instance were included in a new national monumentit was clear that more than 50 years of military use had caused less damage to wildlife than had recreational use on adjoining lands. In other words, decades of low-flying jet fighters and helicopters, bombs and machine-gun fire were less destructive to the landscape and wildlife than were legions of our bushwhacking civilians with their all-terrain vehicles, dune buggies, indiscriminate shooting and neglected campfires. Now I am certainly not suggesting we put elephants or other large mammals out on bombing ranges, active or inactive. Protection zones will obviously never be used for munitions testing or maneuvers. Again, their value is in their relative lack of disturbance. But it is not a far leap from realizing that the military will be setting aside and protecting large stretches of the landscapeto realizing that they might well partner with us in safeguarding populations of species in need of help. Why not work with the military, then, to establish a network of elephant refugia in protection zones? Of course, we will have to work through masses of questions: All the animals physical and psychological needs will have to be met: space, food, water, shelter, security. Research? Veterinary care? Range rest and rotation? Yes. And what about the 10,000 other details? Yes, of course. We will need to negotiate everything with an emphasis on reconciling the well-being of the animals with the requirements of the military. We would need some mechanism for rotating grazing areas and mitigating environmental damage, for providing supplementary food, constant and reliable water, mudbaths and shade during North American summers as well as heat and shelter from the winter nights. These refugia would also be used for new generations of low-intensity training, research and behavioral enrichment. The purpose of the refugia is to allow the animals to establish multigenerational herds which demonstrate social behavior as close to normal as captivity can. This includes raising their young to adulthood. The purpose of these refugia is not to provide young elephants for urban exhibition. And againto be of value to the militarythese protection zones need to be all but free of human use and occupancy. In any possible collaborations with the military, their primary concern will be protecting this usefulness. This means they will be acutely focused on any conceivable compromise of security and safety. As a result, proposals for the use of protection zones will have to meet strict requirements concerning entrance into such zones for management purposes. This means no unwarranted interference with the animals. This also means no animal theme parks. Anyone who thinks this will be simply another marketing strategy is utterly missing the point. No adjoining conference centers with elevated observation areas and animal shows. No five-star tree houses. No VIP jeep tours or luxury tented campgrounds for anyone who can pay the price. No civilian helicopter flyovers! Such refugia will mirror natural circumstances as closely as humans can accomplish. The goal is to enable elephants and other species to live their lives mostly undisturbed, as naturally as captivity will allow. The purpose is to focus on them, to conserve themto guard them, to preserve them, to allow them to survive us.

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* * * It is, however, more than a question of degree. It is a question of courage. And if we can make such a cosmic leap, if we can manage to perceive elephants as intelligent, sentient, complex and miraculous creatures, maybejust maybewe can extend that same respect toward other forms of life. Who knows? Perhaps even to one another. Can urban zoos transform themselves to enable such outcomes? Can we progress beyond our cherished, comforting platitudes? Can we really mean what we say when we declare education, conservation, research, and recreation? Can we pioneer a new era of stewardship of nature? With the military? With universities, corporations, private interests? Can we think differently, in new dimensions? I believe we canif we are bold enough to so choose.
http://www.davidsuzuki.org/About_us/Dr_David_Suzuki/

Reference

The observations in this essay are mine. They are not necessarily those of The Arizona Zoological Society. J. W.

Jeff Williamson is the President of the Arizona Zoological Society and the past director of the Phoenix Zoo. He has also worked at the Brookfield Zoo and Miller Park Zoo and engaged in field work throughout the arid Southwest, Mexico and Central America. He attended Vanderbilt University and did graduate work in Public Policy at Illinois State University. He serves on the Board of the Arizona Wilderness Coalition, Cienega Watershed Partnership, Friends of the Ironwood National Monument, the Board of Advisors for the Trust for Public Lands and Las Fuentes Health Care Center. Jeff may be contacted at The Arizona Zoological Society, 455 North Galvin Parkway, Phoenix, AZ 85008 or at JWilliamson@thephxzoo.com.

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Afterword Celebrating Our Future With Elephants


Paul F. Waldau Center for Animals and Public Policy Tufts University Cummings School of Veterinary Medicine It is often said that elephants never forget. Our own species, frankly, is less gifted with memory. Some of our ancient ancestors learned so much about elephants. They memorialized what they learned in song, verse, myth, scripture and even lengthy treatisesa fine example is the Hindu Hastayurveda. Nevertheless, over time an astonishing amount of our best learning and the wisdom it prompted have faded from memory. This volumes multifaceted discussion regarding science and elephants well-being offers, among other things, the chance to renew and recollect, even recapture, the best of our accumulated wisdom about possibilities in our relationship with these extraordinary animals. We need such wisdom as we contemplate todays realities of the human-elephant story. We also need it as we engage future possibilities. Some of our forebears vacillated in their vision of elephants, in a sense reshaping it again and again as centuries passed. In 1933, the Belgian travel writer, poet and painter Henri Michaux pointed out that over the centuries Chinese writing had adopted eight different shapes for elephants. Originally, it had a trunk. Several centuries later it still has one. But in the meantime the poor animal was made to stand upright like a man. Some time afterwards it lost its eye and its head; still later the body disappeared, leaving only one of the feet, the spinal column, and the shoulders. Later it recovered its head but lost everything else except the feet; and later still it became twisted into the form of a snake. Finally it became whatever you like: it has two horns and a teat emerging from a foot (Jean 1992, p. 187, citing Michaux 1933). This series of changes illustrates nicely the richness and chaos in our views of elephants. It also suggests both how formative and how destructive we can be. But in the midst of all this there is a constantthat humans have long had a special relationship with elephants. An object of worship, a target of hunters, a beast of burden, a burden to the people, gentle in captivity, dangerous in the wild, the pride of kings, the companion of mahouts, a machine of war, an envoy of peace, loved, feared, hated, the elephant has had a glorious and an infamous association with man in Asia. For its sheer contrast and splendour, this association is unequalled by any other interaction between animal and man in the world (Sukumar 1989, p. 1). To achieve a clear and accurate picture of this association, as well as a view of elephants that helps us take their realities seriously in ways that the ever-morphing Chinese characters could not, we need several things. Surely, a leading role must be taken by the many kinds of science reflected in this book. But we need something else as wella renaissance of the human spirit, perhaps a fundamental recollection of what we have always known, as Plato long ago suggested in his famous
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dialogues. What is needed is a shift in world view in the traditions of Copernicus, Newton, Darwin and Einstein. We need to value elephants in and of themselves, not merely as property to be exhibited for someones financial benefit or for our childrens amusement or education. Few would deny that we are capable of seeing elephants as fellow individual beings that share our Earth. Such a renaissance in our views of elephants and its implicit affirmation of our obligations as moral beings to see them as valuable in and of themselves would enrich the human race in ways that far outstrip other considerations such as the economic boons elephants now bring to some of us. Throughout, this book honors the importance of science. As it does so, it also underscores that something is happening with elephants. The growing types of awareness that are reflected in this bookscientific, social, practical, moralare anchored, of course, in the extraordinary features of elephants themselves as biological individuals. These changes in awareness are also related to the complex problems that elephants experience as individuals in captivity. That something is happening with elephants reflects a fundamental feature of todays human community. This can be pictured as foreground in relation to a larger background. That background is like a ferment bubbling up in our society as we re-evaluate the mysterious and rich relationships we share with our nonhuman cousins. The background ferment is driven by a constellation of changes, including shifts in environmental awareness, increases in levels of affluence, rising concern for habitat destruction and its related decimation of species and nonhuman communities, and developing awareness that many human cultures have in the past featured a deep fascination with the more-than-human world (Abram 1996). In the foreground, there is increasing knowledge about and concern for those nonhuman animals whom human individuals can see, touch and relate to as individual personalities playing discernible roles within their own unique communities. Among easily observed animals, elephants are among the most obvious candidates for our scientific inquiries and ethical concern. One result of the ferment is that attitudes in modern societies around the world regarding other animalsother because we, too, are animals in every sensehave undergone important shifts in the last decades. These shifts have been buttressed by scientific discoveries concerning the realities of other animals: their personalities, cognition, communication, emotions, social complexities and even culture.1 Outside science, the ferment manifests in many ways; for example, it appears in professional organizations, the arts, law and the humanities and social sciences. Consider the professional associations that have added sections or focus groups dealing explicitly with nonhuman animals: 1980 American Philosophical Association, Society for the Study of Ethics and Animals 1997 American Academy of Religion, Animals and Religion Consultation 1998 American Association of Geographers 2002 American Sociological Association, Section on Animals and Society 2004 American Bar Association, Animal Law Committee 2007 American Psychological Association, Human-Animals Studies section within the Society of Counseling Psychology (Division 17)
1. One of the stunning contributions of modern primatology has been a close examination of our cousin great apes actual realities in their natural contexts. A volume edited by Richard Wrangham, chairman of the biological anthropology department at Harvard University, describes researchers findings in the tradition of good, careful, rigorous science. The book reveals that scientists now regularly use the prized word culture of all chimpanzee groups. See Wrangham RW.1994. Chimpanzee Cultures. Cambridge, MA: Harvard University Press in cooperation with the Chicago Academy of Sciences. 237

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Animal topics have also influenced the arts. The New York Times, which on June 24, 2000 featured the headline Animals have taken over art, and art wonders why,2 described myriad ways that both nonhuman animal images and themes and even live animals themselves have been included in an astonishingly wide range of modern art. Fundamental changes have occurred in the area of law. Litigation, legislation and administrative regulation around the world suggest increasing concern for elephants. Litigation and court rulings have brought the problems of many animals, including elephants, to public attention. For example, as Robert Marquand noted in a Christian Science Monitor article on February 8, 2000, a Sri Lankan court in a November 1999 decision gave rights to elephants, including happiness, roaming space, and a full belly. Similarly, on June 6, 2000, three judges in the Indian State of Kerala handed down an opinion for the High Court that addressed the plight of elephants and other circus animals housed in cramped cages, subjected to fear, hunger, pain, not to mention the undignified way of life they have to live.3 The court ruled that these nonhumans were beings entitled to dignified existence within the meaning of Article 21 of the Indian Constitution, which protects the right to life with dignity. The courts opinion asked simply, If humans are entitled to fundamental rights, why not animals? The reasoning and conclusions in these legal cases are suffused with the cultural assumption of the Indian subcontinent that elephants are clearly important beings. Different cultures views of these living beings are now being studied widely, a phenomenon that has made clear that many cultures have discerned the remarkable abilities of elephants. Extensive engagement with other often non-industrializedcultures respect for nonhuman lives has made it possible to argue that caring about other animals is also vital to human health in industrialized cultures. This creates more options for those who feel that an ethically-informed and scientifically-based approach to elephants is crucial. The attention now paid in many circles to the myriad ways that human societies have affirmed the importance of elephant and other nonhuman lives and communities has borne fruit in a variety of ways. Even in those countries where mainstream society rejects animal rights, 4 the legal system reflects significant ferment in other ways. In the United States, for example, the biggest legal changes have been in legislation and education. Each year in American legislation, scores of bills, regulations, popular initiatives and other proposals attempt some sort of change or ban at federal, state and municipal levels. Some are profoundly important, such as state-wide bans on certain animal farming practices, while others are symbolic, such as Rhode Islands switch in 2001 from the term owner to guardian.5 In curricula for legal education, the subject of animal law has expanded dramatically. Of
2. Sarah Boxer, Animals have taken over art, and art wonders why, The New York Times, June 24, 2000, pp. B9 and B11. 3. See the case N. R. Nair v. Union of India, 2000 All India Reporter (Kerala) 340-354; the quotes are on p. 353. 4. The term is in quotes because it is an almost meaningless term given the diverse and vague ways that it is employed. As a practical matter, its meaning must always be carefully specified if one seeks good communicationthe term is widely employed to mean at least the following: (1) specific legal rights for some animals, (2) general moral rights for some or all nonhumans, or (3) the general animal protection movement ranging from demands for immediate abolition of long-standing practices to lobbying for amelioration of the most egregious abuses of modern factory farming. 5. The law amended by Rhode Island House Bill H 6119 is available at http://www.rilin.state.ri.us/Statutes/ TITLE4/4-1/INDEX.HTM. See, for examples, Section 4-1-1(4). 238

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the approximately 200 American-Bar-Association-accredited law schools, as of mid-2007, at least 89 offered an animal law course.6 This represents an eight-fold increase in the last decade. This is significant, socially and professionally. While veterinarians are trusted deeply by the public because they are seen as advancing healing and advocating protection of nonhuman animals, the veterinary professions national and state-level institutionsthe American Veterinary Medical Association and the state veterinary medical associationshave opposed rather than advocated changes in the legal status of any nonhuman animals, which are mere property or legal things under the American legal system (Waldau 2007). The upshot is that another professionor, more accurately, the students of the law professionhave now taken up the cause of (nonhuman) animals (Waldau submitted). The upheaval in these broad features of our human communitys relationship with our fellow animals shows up clearly in local veterinarians emphasis on the human-animal bond. In the last four decades, this highly successful campaign has touted the value of humans relationships with companion animals, such as the human-dog or human-cat relationship. Viewed as family relationships, these human-animal bonds have been so heavily emphasized in contemporary veterinary medicine that this more animal-sensitive approach to companion animals now competes with the original, almost exclusively human-centered dimension of the profession that began in the 18th century when the profession was formed to take care of the militarys horses.7 The modern Western veterinary profession has been opened up by this trend in ways that go considerably beyond the professions human-centered origins. The preoccupation with companion animals reflects a continuing preoccupation with human affairs (because the defining feature of companion animals is their relationship to humans), but the following comment about wildlife made by a leading veterinary ethicist suggests an expansion of concern throughout the profession that clearly opens the door to Abrams more-than-human world: There appears to be virtually universal enthusiasm among veterinarians about the professions growing involvement in the treatment and protection of wildlife (Tannenbaum 1995, p. 527). Changes in our societys willingness to engage some nonhuman animals has influenced the academic and scholarly world as well. One now easily finds, in a wide range of fields other than those with a strict biological orientation, tremendous interest in species other than our own. Each year brings new contributions on other animals from scholars in religion, philosophy, history, literature, geography, sociology, anthropology and even politics.8 The ferment in views about nonhuman animals has in fact produced several new academic fields, all of which are part of the emerging
6. A list of animal law courses can be viewed at http://www.aldf.org/resources/details.php?id=297. 7. Dunlop and Williams in their helpful Veterinary Medicine: An Illustrated History (1996, St. Louis, MO: Mosby) point out (p. 349) that the first veterinary schools were set up in the late 18th century to meet military needs to keep horses operational. 8. See, for example, the following books in these fields: Waldau P, Patton K. 2006. A Communion of Subjects: Animals in Religion, Science, and Ethics. New York: Columbia University Press; DeGrazia D. 2002. Animal Rights: A Very Short Introduction. Very Short Introductions: 57. Oxford: Oxford University Press; Anderson VD. 2004. Creatures of Empire: How Domestic Animals Transformed Early America. Oxford; New York: Oxford University Press; Baker S. 2001. Picturing the Beast: Animals, Identity, and Representation. Urbana, IL: University of Illinois Press; Wolch JR, Emel J. 1998. Animal Geographies: Place, Politics, and Identity in the Nature-Culture Borderlands. London; New York: Verso; Nibert DA. 2002. Animal Rights/Human Rights: Entanglements of Oppression and Liberation. Lanham, MD: Rowman & Littlefield; Anderson EN, Tzuc FM. 2005. Animals and the Maya in Southeast Mexico. Tucson, AZ: University of Arizona Press; Garner R. 2004. Animals, Politics, and Morality. Issues in Environmental Politics. 2nd ed. Manchester, UK; New York: Manchester University Press/Palgrave. 239

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super-field of human-animal studies. Publications such as The Chronicle of Higher Education have, for example, featured articles on multi-disciplinary fields like anthrozoology (Malamud 2003). Significant social effects have emerged from this ferment: animal shelters work hard to place abandoned animals rather than euthanize them; churches feature many more ceremonies focusing on animals; corporations advertise their involvement in animal protection projects; researchers conduct memorial services for experimental animals and the number of animal volunteer groups has increased dramatically. Changes in so many different areas of society give added significance to the developing debate about our relationship with other animals. The informed public holds elephants in particular to be a cause clbre for many reasons: each is easily understood to be not only a remarkable individual but also a discernibly unique one; our devastation of them as a species is an easily comprehended example of the harm we are bringing to so many other species on the planet; and elephants intelligence and social complexity are easily demonstrated, casually and scientifically. All of these reasons make elephants personally appealing to us as members of another eminently social species. Beyond these reasons for celebrity, though, elephants have an added significance. They represent well our possible relationships with the more-than-human world. As a keystone species in nature, elephants are also a keystone in our own thinking about the natural world. Indeed, elephants are good to think, as the anthropologist Lvi-Strauss famously said of nonhuman animals (1963). Their evident intelligence and surpassing physical strengths allow them to challenge us as they seek to meet their basic ecological, familial and individual needs. They are very unlike our domesticated dogs and cats, which have become family because they are dependent upon us. Elephants, though they are losing the battle with our species, have been in a very real sense our competitors, often our equals, and even at times our betters. This rich relationship, with all its complex allure and challenges, is what spurred Sukumars multifaceted description quoted above. In so many ways, then, elephants test our spirit. Our ability to respect them, and in particular our ability to let them be elephants without reshaping them, epitomize something one of the 20th centurys great theologians said: Indeed we cannot be truly ourselves in any adequate manner without all our companion beings throughout the earth. The larger community constitutes our greater self (Berry 2006, p. 5). Wreaking devastation on elephants in the wild, holding captives in ways that produce anthropogenic illnesses and treating these unique, eminently social individuals as mere legal property that can be bought and soldall of these habits and practices suggest a great deal about us, including a lack of collective vision, inherited institutional insensitivities and a tendency to ethical blindness. For some, such practices betray cultural impoverishment and even portend our species moral bankruptcy. Questions about our relationships with elephants, then, interestingly reflect ways in which our society is recalling perspectives that our ancestors sometimes achieved. Our forebears views of other animalsand most certainly of elephants when they were knownreflected, it should be remembered, a deep conviction that human interactions with many nonhuman animals were of great significance morally. They often saw other animals as bringers of blessings (Paulson 1964) or even as other nations deserving of respect (it is interesting, for example, to compare the abundant references to other animals as nations in, say, Native American materials with the Islamic claim (in Quran 6:38) that all other animals have their own communities). This special feature of ancient peoples human-animal relationships by no means prevented them from hunting other animals, but it surely led to fundamental respect for many nonhuman animals in the vast majority of ancient cultures. It is thus natural and in a sense respectful of our ancestors to raise the question of current
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practices. What, in fact, is our treatment of elephants? Can we inhabit the earth together, in ways that meet their needs and ours? To answer such questions accurately, we require sciencegood information about their lives in nature in order to assess the character of their captivity by us. We also need this information to assess what the right courses of action might be in the future. With good information, we have a chance to rememberand then never to forgetwhy some ancient humans honored elephants, feared them as well, and knew at the same time that it was inevitable that these and other nonhumans play an exquisite role in healthy humans lives. Elephants thus, so powerful and competitive with us, force one important question after another: if not here and now, where and when else could we bring alive a deep compassion for these extraordinary nonhumans? Our scientific and ethical abilities can work in combination to allow us to glimpse possible futures. A world with healthy, stress-free elephant families and societies is a rich world, indeed. A world inhabited by distressed elephants is not unlike a world without them; it is an impoverished world. Until we see our own past, and the biases and rationalizations we have inherited that favor captivity premised on anthropocentric justifications, we will not see what or how much is possible in the future or in our own natures. The future is better seen if we understand what is now limiting our imagination. It is precisely our inheritance of easily rationalized captivity that shackles us. While our inheritance regarding elephants is, of course, that we have often harmed them, we can surely choose to change this, to opt for the prospect of a deeper understanding of our possibilities with elephants. To paraphrase the noted social change and democracy activist Frances Moore Lappe: Every choice we make regarding elephants can be a celebration of the world we want. To see the futures parameters, one does well to ponder todays polarized debate. Although most wish to find a better future, people at one pole advocate abolition of captivity altogether even as those at the opposite pole accept the tradition of captivity we have inherited as nonproblematic. In the midst of the great polarization about elephants it is wise to look for common ground. One candidate for a consensus view is a straightforward, uncompromising recognition that elephants are profoundly important and matter in and of themselves. On such common ground stand many who handle and otherwise manage elephants; some others who own elephants as property under current law also share this view. On this common ground, too, stand those who would help change our present forms of captivity to something better. Recognition that elephants matter in and of themselves is also a key claim of those who do not find captivity a moral option unless it is truly a matter of life and death for an individual or group, and then only for the briefest time in the most benign of circumstances. But can the human community reach this common ground? Chances are, given our own species long, complex and morally troubled history with other animals generally, some people will continue to deny that elephants truly matter. Such is the byproduct of growing up in cultures and under legal systems that radically subordinate any and all nonhuman interests to virtually any and all human interests, however trivial. But such objectors to the proposal that elephants matter in and of themselves may well be outvoted in future public policy discussions because of increasing recognition that elephants do in fact matter. Who today wishes to stand up for the proposition that our human community cannot, as a whole, proceed to a better future based on our shared commitment to protect elephants as important to the future of Earth, our childrens world and our own integrity? The way forward is at least this clear: the human community needs a scientifically informed
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view of elephants and of our captivitys effects on them. With this information, we can repair our own current ignorance about them. With this information, too, as it works hand-in-hand with an ethically sensitive vision of how individual human communities might live with elephants in the most benign of ways, our larger human community can plan a specific, realistic future. It will help if we undertake these important tasks humblyif we recognize that each of us was born into a society that callously accepted elephants captivity in ways that harmed, even reshaped, individual elephants as radically as did the Chinese characters. It will help if we accept the pain of admitting that our society has through captivity clearly sickened many elephants and turned many of them insane. Consider this moving passage about the fate of an elephant that one Buddhist king attempted to honor: And he rocked, constantly, tugging on chains that bound his legs to the slightly raised platform on which he stood[T]his bull was never let out of the pavilionSo for decades now, he had been here on his raised dais, rocking, straining, surging back and forth with unfathomable powerSurging, swaying, pulling this way and that, forever and a daythe heaven-sent king of elephants, born of clouds and rain, colored like the sacred lotus, a captured god but now an obsolete one, something out of a distant time and kingdom, his purpose all but forgotten[A]lone in his dark, golden-spired pavilion. Forever alone. Colossal. And very likely insane. That was the message in those eyes: madness (Chadwick 1994, pp. 352-3). It is, in particular, our next step that counts. The past is what it is, and we do well to learn from it in ways that ensure bad things cannot happen again. In the face of our ugly past of harming elephants in many ways, who today can make any sort of informed, cogent, morally sensitive argument that our societys response to elephantsscientifically, ethically, culturally, politically, institutionally, educationallyshould not be controlled by elephants actual realities? Can there today be any morally respectable argument that the controlling factor in future decisions regarding elephants should be restricted to human self-interest? It is both our scientific and ethical natures that press questions about elephant well-being. In precisely which situations does our method of holding elephants in captivity affect too much of the lives of individuals? Can we find a way to hold without harm those individual elephants who cannot now be returned to the wild? If we succeed in answering such questions well, we may finally recall what our ancestors knewour species is accompanied on this planet by these remarkable nonhumans. If we reach this realization, then yesterdays and todays elephant captives will have been emissaries to us in several ways, as ambassadors for their free-living cousins and for the wild or more-than-human world, as well as heralds for many other nonhumans. Yesterdays and todays captive elephants will have brought us the message that their lives, too, are important. They will have taught us that when we accommodate them, we thereby enrich all animals, human and nonhuman alike. Elephants can thus be the harbingers of our own better future. In the highly polarized environment of the present, we must protect those who state this vision. The Tufts Symposium was designed as a safe haven where people of good will could be realistic about the nature of important questions like best management practices. Such questions, unavoidable from scientific, ethical and planning standpoints, have an undeniable power. In the end, such questions coalesce into simple pleas: what is, what has been, what might be the role(s) of humans in caring about elephants? Where, if not here, can we bring compassion for captive elephants alive? When, if not now, can we ask about the effects of our captivity on them? Why, if
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not here and now, can this dialogue not begin in earnest? This volume takes important steps towards answering the questions abovemay it give further voice to an open-minded and optimistic approach to assessing the future of elephants in captivity. References

Abram D. 1996. The spell of the sensuous: perception and language in a more-than-human world. New York, NY: Pantheon Books. Berry T. 2006. Loneliness and presence. In: Waldau P, Patton K, eds. A communion of subjects: animals in religion, science, and ethics. New York, NY: Columbia University Press. p. 5-10. Chadwick D. 1994. The fate of the elephant. San Francisco, CA: Sierra Club Books. Jean G. 1992. Writing: the story of alphabets and scripts. New York, NY: H.N. Abrams. Lvi-Strauss C. 1963. Totemism. Boston, MA: Beacon Press. Malamud R. 2003. How people and animals coexist. Chronicle of Higher Education, Vol. 49(20):B7-9. Michaux H. 1933. Un barbare en Asie. Paris: Gallimard. Paulson I. 1964. The animal guardian: a critical and synthetic review. Hist of Religions 3(2):202-219. Sukumar R. 1989. The Asian elephant: ecology and management. New York, NY: Cambridge University Press. Tannenbaum J. 1995. Veterinary ethics: animal welfare, client relations, competition, and collegiality. 2nd ed. St. Louis, MO: Mosby. Waldau P. 2007. Veterinary education as leaderwhich alternatives? J Vet Med Edu 34(5): 605-614. Waldau P. 2008. Submitted. Review of ethics and law education in veterinary schools with respect to the human animal bond. J Vet Med Edu.

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Appendix I Optimal Conditions for Captive Elephants 2005 Lisa F. Kane, J.D. Debra L. Forthman, Ph.D. and David Hancocks

Updated 2007

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Caveats....................................................................................................................................248 1. Introduction....................................................................................................................248 2. Scope...............................................................................................................................249 3. Assumptions....................................................................................................................249 4. Discussion........................................................................................................................249 4.1 Assessing elephant welfare in zoosan overview................................................................249 4.2 Zoo management models.................................................................................................250 4.3 Managing captive elephants as unique members of a population......................................251 4.4 Waldaus approachassessing captive elephant welfare in light of key individual characteristics and the species natural history .................................................................252 4.5 Applying Waldaus approachdefining elephants key characteristics................................253 4.6 Cognitive ability...............................................................................................................253 4.7 Social complexity.............................................................................................................254 4.8 Physical vigor ...................................................................................................................257 4.9 Optimal conditions of captivityHedigers perspective on the captive environment and Eisenbergs model of mammalian life strategies..........................................................258 4.10 Delivering optimal conditions of captivity........................................................................258 4.11 Definitions.......................................................................................................................259 4.12 Physical variables.............................................................................................................259 4.13 Physical variables and elephants.......................................................................................261 4.14 Sensory variables .............................................................................................................261 4.15 Sensory variables and elephants........................................................................................262 4.16 Occupational variables.....................................................................................................263 4.17 Occupational variables and elephants...............................................................................263 4.18 Feeding variables..............................................................................................................263 4.19 Feeding variables and elephants........................................................................................264 4.20 Social variables.................................................................................................................265 4.21 Social variables and elephants...........................................................................................265 4.22 The human-elephant relationship.....................................................................................266 4.23 Definitions.......................................................................................................................266 4.24 Free contactselected topics...........................................................................................267 4.25 Protected contactselected topics...................................................................................270 4.26 Passive controlselected topics.......................................................................................272 5. Analysis................................................................................................................................273 6. Recommendations ...............................................................................................................275 References................................................................................................................................276
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Caveats Minimal research measuring captive elephants welfare and behavioral issues has been conducted in North America. Most of the studies cited here and in support of the Coalition for Captive Elephant Well-Beings specific model Best Practices (Appendix II) were conducted with laboratory animals. Where scientific evidence in various situations suggests a range of measurable results from no distress to acute distress and where there are no definitive elephant studies, we have chosen to rely on studies of other animals until scientific studies directly related to elephants in captivity demonstrate the absence of distress in the relevant situation. It is outside the scope of this chapter to address the destructive impact of human activity on free-ranging elephant populations that is evident throughout most of Asia and Africa. Nevertheless, we are mindful of the daily hardship and danger faced by free-ranging elephants. Their plight is often desperateeither due to degraded environments into which they are pushed or the lethal consequences of competing with humans for space and other resources. The existence of such circumstances does not affect the accuracy of the scientific evidence underlying this document.If anything, their struggle in the wild makes the Coalitions quest to preserve their lives and history all the more urgent. We (and the Coalition) take no position on the value of exhibiting captive elephants. That, as well, is outside the scope of this chapter. We understand that theoretical and applied forms of research are distinct, although both are often empirical. We believe that both literatures are useful in determining the nature of optimal conditions of captivity for elephants.In this document, we examine and rely on the theoretical work of Paul Waldau, Heini Hediger, John Eisenberg, John Seidensticker and James G. Doherty. While they are certainly not the only contributors to this field, we believe their models and analytic approaches to captive wildlife in general, and elephants in particular, are helpful. Viewed together, their works offer a unifying framework into which to fit the important elements of husbandry and management of captive elephants. The scope and thoroughness of their thinking allow us to make reasonable judgments about optimal conditions where no evidence exists at the present time.Finally, their visions free us from the conventions of traditional industry practices. 1. Introduction As of September 2004, AZA-accredited (American Zoo and Aquarium Association) institutions held 133 African elephants scattered throughout the country in groups of unrelated individuals. Approximately 148 Asian elephants are held in similar circumstances at AZA zoos (Keele 2004). The most notable result of captive elephants flagship status in zoos is the zoo communitys commitment to breeding reproductively-viable animals and to importing elephants from the wild. In short, there is reason to believe that elephants will be exhibited in zoos throughout North America for many years to come. To date, no comprehensive evidence-based context for developing standards of care has been reported in the literature. In addition, current AZA elephant management standards are minimal and, in the authors opinion, are generally not supported by current scientific evidence. This document is intended to provide a different visionan evidence-based foundation for model best practices for use by the zoo industry, non-zoo institutions such as sanctuaries, and government agencies that license or otherwise oversee such institutions. This project is driven by two major assumptions: (1) elephants in captivity are most likely to flourish in an environment
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that provides conditions promoting species-appropriate behavior as revealed by the species natural history; and (2) a training regime predicated on positive reinforcement and respect for the animals autonomy is best suited to enhancing the lives of captive elephants and providing for their psychological well-being. 2. Scope Here we review and analyze the present state of scientific knowledge of elephant behavior in the wild and identify critical elements of an optimal captive environment that might encourage the expression of natural elephant behavior when welfare is a prime consideration. We also analyze in some detail one aspect of the captive elephant environmentthe humanelephant relationship. This document describes three management systems in use: free contact, protected contact and passive control. We identify the tools, techniques and consequences to animal welfare and keeper safety associated with each system. This section also discusses the unique properties of positive reinforcement training that promote captive elephant welfare in contemporary American zoo facilities. 3. Assumptions This document is intended to be the foundation for and companion to the Best Practices for Care and Well-Being of Captive Elephants of the Coalition for Captive Elephant Well-Being (Appendix II). The Best Practices document rests on four assumptions: 1. Elephants in captivity should be managed as unique individuals as well as members of their respective populations. 2. Design of captive environments, whether zoo exhibits, sanctuaries or any other constructed environment that encloses and restrains elephants should emphasize the needs that an elephant itself perceives to be important (Mench & Kreger 1996, p. 13). 3. Zoos and sanctuaries should provide their elephants optimal conditions of confinement predicated on the critical elements of the species natural history and elephants key individual characteristics (Hancocks 1996; Coe 2003). 4. Management best practices for elephants in captivity should incorporate training principles that: maximize the elephants learning, autonomy and competence; minimize their experience of unnecessary pain or distress; and maximize keeper safety. 4. Discussion 4.1 Assessing elephant welfare in zoosan overview Animal welfare is a function of a constellation of variables, including behavior, health, reproduction, and longevity (Laule 2003, p. 969). Zoos undoubtedly deliver timely and appropriate veterinary care. Still, elephants in captivity exhibit low reproductive success when compared to elephants in the wild (Moss 1988; Taylor & Poole 1998; Olson & Wiese 2000; Wiese 2000; Rees 2003). Further, even under the most favorable statistical assumptions, the longevity of zoo elephants is not better than that of free-ranging elephants (Wiese & Willis 2004; Lee & Moss, Chapter 2). This is true even though zoo elephants are protected, for example, from the two main causes of early death in free-ranging African elephant populations: drought and human predation
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(Moss 1988). Setting longevity and reproductive rates aside for the moment, the most significant daily distinction between the lives of free-ranging elephants and their cousins in captivity is the virtual absence of opportunities for zoo elephants to engage in the repertoire of behaviorssensory, occupational and socialnormal to their species (Clubb & Mason 2002). As Desmond (1994, p. 19) suggested a decade ago, Pursuit of enhanced animal welfare depends on assessing our efforts in terms of the animals behavior. In other words, the delivery of optimal care in captivity would be reflected in captive populations of elephants exhibiting a full range of natural behaviors. Under Desmonds measure, zoos are not providing optimal welfare for the elephants in their care, despite the fact that great strides have been made to enhance the behavioral management and welfare of other species kept in zoos (Kane, Chapter 7; Maple, Bloomsmith and Martin, Chapter 10). The reality of life for many zoo elephants is confinement with one or two unrelated individuals in a spatially limited environment that is sterile and unchanging, in comparison to the wild (Laule 2003, p. 969). Virtually all elephants in captivity are denied natural family groups. It therefore comes as no surprise that few zoo elephants are socially or reproductively competent when compared to their wild counterparts (Rees 2001). 4.2 Zoo management models Seidensticker and Doherty (1996) provide useful schema for thinking about animal welfare and management in zoos. They describe four approaches: 1. The zoo exhibit animal management model is summarized by the phrase, Zoos are for people. This model encompasses those zoos today that, like their 19th-century counterparts, display animals for close inspection by zoo visitors and use their animals in shows and for rides. 2. The medical management model emphasizes direct human technological intervention to help animals in captivity remain healthy. It focuses on fixing animals so that they can adjust to conditions of confinement rather than adjusting the conditions of confinement. 3. The ethological model is summarized as Zoos are for wild animals that move and do things. This model is based on the notion that zoo animals should be managed so that their lives differ as little as possible from those of their wild conspecifics. 4. The humane animal management model assumes zoos are welfare states responsible for the care of individual animals from cradle to grave. This model is unconcerned with the zoo visitor and with animal species or populations as a whole. This model is sympathetic to many aspects of the ethological model, but not to any ethologically related practices that might be perceived as potentially injurious or stressful to individual animals. The humane animal management model dictates that animals can choose whether they want to be on exhibit or off, a choice that confounds exhibition strategies. From a functional point of view, applied behavioral conditioning including positive reinforcement can serve the goals of any and all four approaches to animal management and welfare in zoos. We believe a balance of the best features of the third and fourth approaches is most likely to result in a humane and effective management philosophy and the provision of optimal conditions
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of confinement (Forthman 1998). The third approach (the ethological model) embraces the assumption that institutional recognition of the species natural history and key characteristics of individuals is crucial to providing healthy, optimal conditions of confinement. Such recognition places responsibility squarely on all levels of zoo management to adjust conditions when reasonably possible to meet the animals needs. The fourth approach (the humane animal management model) puts the interest of the individual animal first and foremost. This premise is the first value informing humane animal welfare and animal management.1 Accordingly, this value in the humane approach serves as the tiebreaker in those situations where competing interests dictate differing approaches and outcomes.2 4.3 Managing captive elephants as unique members of a population AZA zoos manage their small populations of elephants from a species perspective (Hutchins, Smith & Allard 2003). The central goal of this top-down approach is to enhance the species health and reproductive vigor. This intention is put into practice through AZAs Elephant Management Standards (EMS), which mandate extensive and invasive veterinary protocols intended to promote zoos ambitions to breed their elephants (AZA 2003). Within the last year or two, AZA Species Survival Plans (SSP) breeding recommendations frequently have required individual animals, almost always females, to move from institution to institution with little obvious regard to aspects of the individuals welfare3 beyond her potential as a cycling female. Other movements of female elephants and the concomitant disruption of established relationships between bonded animals have been justified on the ground that one of the animals will fulfill an important social role in its new group.4 Frequently, such experience and knowledge is wholly absent from the animals history because the elephant was separated from her natal herd in the wild as a young calf and spent her life as a member of a small, unnatural pair or group of unrelated, possibly equally socially disadvantaged individuals. An impoverished social background, common to most AZA zoo elephants, does not equip them to discharge the complex reproductive or social roles their transfers are frequently intended to accomplish (e.g., Bradshaw, Chapter 4; Poole & Granli, Chapter 1). One of the consequences, then, of AZAs management of its elephants from a species perspective, is to minimize the welfare needs and history of its elephants as individuals (Hutchins et al. 2003). This policy approach has produced an aging population of Asian and African elephants who, by the AZAs own admission, cannot sustain their small numbers (Olsen & Wiese 2000;
1. The well-being of captives is a subject that will always be susceptible to the imposition of human values (Maple, McManamon & Stevens 1995). 2. We believe that zoos holding elephants have the responsibility to inform the public of the true costs and ongoing financial burden of providing their elephants optimal conditions in captivity. This educational process may help the public and zoo administrators realistically assess their ability and willingness to undertake the expense, responsibility and commitment necessary to exhibit elephants in optimal conditions. 3. For example, three elephants that had lived for 30 years with daily access to a multi-acre outdoors exhibit were transferred at respective ages of 54, 34 and 34 to another facility and expected to adapt to living conditions that included long, harsh winters and greatly reduced living space. 4. An African elephant that had lived and been bonded with an Asian elephant for over a decade was transferred two thousand miles to a zoo holding Africans. The elephant did not integrate successfully into her new social group and was eventually returned to the zoo of origin shortly before a state court was scheduled to address the propriety of the zoos action in transferring the elephant from her longtime home. 251

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Wiese 2000). A different and potentially rewarding approach would be to view the welfare of individual elephants as the foundation for a flourishing population. As Jamieson pointed out in 1995, [I]t is as misleading to speak of the welfare of a nonhuman species as it is to speak of the welfare of the human species. It is individual organisms that have welfares. As the philosopher Jeremy Bentham wrote nearly two centuries ago, the welfare of a community is simply the sum of the welfares of individuals (Jamieson 1995).5 Today, modern biologists proceed on the assumption that the primary unit of significance in ecology is not the species but, rather, populations composed of unique individuals (Mayr 1976).6 Thinking about AZAs elephants as individuals rather than collectively as a herd or as members of an elephant species more accurately describes zoo elephants experiential reality and is more in keeping with modern principles of biology. Such an approach takes into account each elephants unique genetic heritage and physical, mental, social and psychological history and is more likely to result in the animals enhanced well-being. An approach focused on delivering optimal conditions of confinement as measured by the animals behavior should gradually result in a healthy and flourishing population. 4.4 Waldaus approachassessing captive elephant welfare in light of key individual characteristics and the species natural history Before addressing Hedigers concept of optimal conditions for captive wildlife and its application to elephants, we consider a different prism through which to discern both what captive elephants need and what a captive environment must provide. This is the prism of key individual characteristics. Waldau (2002) postulates that the specific attributes expressed by elephants, such as intelligence and social complexity, may deserve moral consideration. Although the moral weight appropriately attributable, for example, to an elephants intelligence is outside the scope of this discussion, it is useful to consider Waldaus hypothesis as a means to describe the behavioral reality of individual animals. His approach compels consideration of each individual animals reality and, simultaneously, provides a means to assess whether the animal is in an environment permitting it to experience its essence. So, we adopt this prism to the extent that it compels caregivers to focus on the well-being of individual captive elephants and offers an approach by which to define wellbeing for individual elephants. The question Waldau posits and that we adopt, albeit in a different context and with a different purpose, is what makes an elephant an elephant? As a general matter, we know from reports of elephant behavior in the wild (and in captivity) that they are complex individuals possessing distinct histories, personalities and interests (Moss 1988). More specifically, we know that they live in family groups in which they exhibit strong attachments, attachments often lasting a lifetime (Moss 1988; Sukumar 2003). We know elephants are sentient creatures capable of suffering both physically and mentally (Moss 1988). Finally, we know that elephants are physically vigorous creatures that possess the strength and endurance to
5. Darwin recognized this principle, too, when he observed that natural selection operates on the level of individuals, not on the level of a species. 6. A population is subject to mathematical and statistical analysis. It is also true that whatever is measured by such means may or may not be descriptive of or relevant to any given member of a small population (Mayr 1976). As Albert Einstein once remarked, Not everything that can be counted matters, and not everything that matters can be counted. 252

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transform forests into savannas and who move constantly through the large spaces of their home ranges (Poole 1997; Poole & Granli, Chapter 1). An important part of the answer to the question of what constitutes optimal conditions of confinement for elephants is answered by recognizing at least three key characteristics of individual elephants, irrespective of their species. These characteristics are: (1) cognitive ability or intelligence; (2) social complexity; and (3) physical vigor. 4.5 Applying Waldaus approachdefining elephants key characteristics Elephants are complex individuals with distinct social histories: Each elephant is different from every other elephant, not only by virtue of its distinctive genes, but also because it has undergone unique experiences in life (Sukumar 1994, 106). As Waldau points out, apart from the fact that each elephant is an individual in the logical sense, each has a distinctive history in a social context populated by others with distinct histories (2002, p. 78-79). Evidence collected over the past 30 years by field scientists uniformly supports the observation that elephants, as individuals, exhibit significant cognitive abilities, social complexity and remarkable physical vigor (Eisenberg 1981; Moss 1988; Estes 1991; Sukumar 1994; Poole & Granli, Chapter 1). A humane captive environment must reflect an informed understanding of these key characteristics and the putative needs they generate (Mench & Kreger 1996, p. 13; Mason & Veasey, Chapter 11; Poole & Granli, Chapter 1). 4.6 Cognitive ability Elephants show a broad array of behaviors that behavioral scientists associate with intelligence. These include: (1) noticeably different mental states or moods; (2) complex cognitive skills such as using mirrors to locate hidden objects (Vauclair 1996, p. 143); (3) play (Fagen 1981, p. 178-179; Moss 1988, p. 106-107, 112; Shoshani & Eisenberg 1992, p. 134-136; Masson & McCarthy 1994, p. 148-149); (4) boredom (Chadwick 1994, p. 18); (5) deception (Griffin 1992, p. 209); (6) tool use (Vauclair 1996, p. 53; Hart, Hart, McCoy & Sarath 2001); (7) use of medicinal plants to treat wounds and parasites (Douglas-Hamilton & Douglas-Hamilton 1975; Moss 1988, p. 261; Payne 1998, p. 53; Engel 2002, p. 92-108); and (8) potential self-awareness (Gallup 1983; Gergely 1994, p. 55; Poole 1998). An elephants large brain accommodates both impressive capacity for memory storage but also the ability for complex acoustic communication. The acquisition and use of language has long been accepted by behavioral scientists as a mark of superior intelligence. Elephant species demonstrate a relatively large vocal repertoire and extensive communication networks (McComb, Moss, Baker & Sayialel 2000; Poole & Granli 2003 http://www.elephantvoices.org). The complex communication skills of elephants enable them to maintain an equally complex social system. Elephants exhibit skill and experience as they negotiate relationships with many different individuals they meet over their long lives (Poole 2004). For example, an analysis of playback experiments with adult female African elephants suggests that they distinguish infrasonic contact calls of female family members and bond group members from those of females neither in their families nor bond groups. It was further determined that they could discriminate between calls of family units further removed than bond group members, apparently on the basis of how frequently they encountered them. The researchers estimated that, in order to perform the discriminations observed, the elephants studied were familiar with the contact calls of 14 families or 100 adult females in the population (McComb et al. 2000). Elephants learn from experience and pass their knowledge on to younger members of the
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family unit (Sukumar 2003). Recent research suggests that enhanced auditory discrimination skills possessed by the oldest member of a group influenced the social knowledge of the group as a whole (McComb, Moss, Durant, Baker et al. 2001). The capacity to learn and teach is another hallmark of intelligence recognized by humans. Poole argues that elephants transmit knowledge, demonstrate complex emotions and possess a concept of self, a sense of humor and a concept of death (1998). Payne recently agreed that elephant species develop and maintain multiple and many-layered social relationships over long periods of time and through changes in age, status and condition (2003, p. 507-510). Paynes report offers additional evidence of the importance of individuals, as she notes 129 responses to the death of an elephant calf by elephants present in a Dzanga Sangha forest clearing in the Central African Republic. Intelligence, along with a well-developed system of communication that makes use of all sensesauditory, olfactory, tactile, visual and seismic (OConnell, Hart & Arnason 1999)enables elephants to maintain a broad network of relationships involving family, more distant kin, friends, foes and strangers. Elephant intelligence and communication skills help them find mates and consorts, and rear their highly altricial young. 4.7 Social complexity Reproductive competence It is reported that the potential lifespan of elephants is around 50-70 years for Asian elephants and 80 years for African elephants (Walker 1975; Lee & Moss, Chapter 2). In the absence of human predation and drought, wild African elephants can expect to live to a ripe old age (Moss 1988, p. 268). Such longevity has a number of interesting correlates of particular relevance to managing elephants in captivity. As large animals, elephants are a K-selected species (Eisenberg 1981), slow to reproduce even under favorable environmental and social conditions in the wild (Moss 1988, p. 239). The slow rate of reproduction reflects the magnitude of resources required to rear a calf successfully. The lengthy period of dependence of elephant calves requires a considerable investment of energy and attention, not just by the mother, but by the entire family group, as they participate in teaching young elephants the skills they will need to become competent adults. After its birth, a calf will be nursed and tended intensively by its mother for six months. A calf can suckle from its mother or aunts well into its second year. The weaning process is gradual, as the youngster feeds more and more independently over time (Estes 1991). Because Asian calves may also nurse from more than one female, Eisenberg (1981, p. 186) concludes that the presence of many lactating females in matriarchal herds often ensures adequate nutrition for calves. Lee and Moss report that African elephant calves suckled until they were at least 4.5 years old (1986). Lee and Moss also report that, because of the greater energetic investment bull calves require, cows with surviving bull calves tend to have a longer inter-birth interval than those with surviving cow calves (1986). Moss reports that the whole herd assists in rearing the young. Moss observed that a young calf is rarely more than a few feet from its mother, and is often less than one foot away (1988, p. 162). Mother and calf are in almost constant physical contact. Even at 9 years a calf may spend over half the time less than 5 m from its mother (Estes 1999, p. 227). Interactions between calves and other elephants are frequent, involving play, relaxed, friendly greetings or assistance from others when calves are threatened or distressed (Lee 1987). Juvenile and adolescent females in the herd give comfort to, assist and protect calves. These allomothers tend to
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be family members but are not always siblings. Lee notes that siblings maintain close proximity to calves and that calf defense also routinely involves less closely related family members (1987). Lee concludes from her observations that the early establishment of close care-taking relationships within families may enhance the stability of the family through time (1987). Undoubtedly, such relationships support a calf s survival. The onset of puberty in females occurs at around 11 or 12 years of age with first calves born when females are about 13 years old (Moss 1988, p. 34). These first-time mothers receive strong support in calf-rearing from the entire family. Unlike most non-ape species, female elephants live long after reproductive senescence. Estes (1991, p. 261) concludes that their long post-reproductive lifespan reflects the crucial roles that [l]eadership and experience playin elephant social organization The family setting is thus indispensable for the normal growth and development of the young elephantsWithin the family, the calves are protected, nourished, nurtured, and taught the rules of living (Sukumar 1994, p. 102). Females stay with their mothers throughout their lives. These family units are the most stable across seasonal and temporal partitions (Wittemyer, Douglas-Hamilton & Getz 2005). Relying on research conducted by Poole, Moss reports that male African calves reach puberty between 10 and 15 years of age and leave the matriarchal herd anywhere between the ages of 10 and 19, with the average age of independence at 14 (1988, p. 101). Still, young males tend to stay near cow/calf herds, tagging along the periphery with their peers. As they grow older, they gradually move in groups into all bull areas (Moss 1988, p. 112). Bulls typically come into musth at age 30 but compete successfully for females only when they are much older (Moss 1988, p. 112). Males enjoy the society of many elephantsincluding a wide range of matriarchal groupson a regular basis, but do not exercise group leadership (Sukumar 1994, p. 92). Eisenberg also wrote extensively about the influence of Asian elephants social life on their reproductive competence. He observed [t]he initiation of a young elephant into its social unit is a gradual process. He noted that until about four years of age, the social roles of males and females are virtually identical, but they begin to diverge in the fifth year, and from then on we can speak of a separate male role and a series of female roles (Eisenberg 1981, p. 184). Although a male may reach sexual maturity at seven or eight years of age, the average age of onset of puberty is 10-12 years. The young male begins to achieve adult stature and size at 17 years of age, but continues to grow throughout his life. Eisenberg refers to the years from 14-17 as a sub-adult phase. During these years of maturation, a young male engages in contests with members of his own age-class (Eisenberg 1981, p. 184-185). In this way, dominance relationships are established among males who are familiar with each other because home ranges overlap. The contests rarely result in serious injury and seemed to Eisenberg to be limited to tests of strength. Younger males tend to follow and feed in the vicinity of older males. Eisenberg noted that older males with an established position in the populations social hierarchy are generally semi-solitary for the better part of their lives. These field observations of African and Asian elephants offer specific evidence that successful rearing of elephant young occurs over many years in the context of a stable multi-generational herd. This brief literature review supports at least five key observations: (1) an elephant calf s maturation takes years; (2) calf rearing is the main work of the matriarchal herd; (3) the occasion of weaning is not a marker of the calf s physical independence, intellectual development or social competence; (4) after reaching adolescence, female and male elephants go on to lead significantly different lives, the full range of which takes decades to unfold; and (5) the acquisition of social and reproductive competence by adult elephants, whether male or female, also involves a lengthy series of events and experiences.
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Unique social skills of female elephants Female elephants may possess one of the most extensive social networks of any mammal studied other than human primates. It follows that understanding their social organization into multi-generational herds, bond groups and clans is of paramount importance. The fundamental social unit is the matriarchal cow-calf herd or family unit (Wittemyer et al. 2005). Moss (1988, p. 35) notes that the matriarchal herd is, a tight-knit coordinated group generally composed of a mother and her young with her grown daughters and their offspring. African and Asian female elephants remain with their natal herd throughout their lives (Eisenberg 1981; Moss 1988; Estes 1991; Sukumar 1994). The typical matriarchal African herd size is 9-11 (Estes 1991, p. 260). The herd synchronizes its activities such as feeding, or walking, or resting, or drinking or mud wallowing (Moss 1988, p. 35) with the matriarch dictating the activity, direction and rate of movement (Estes 1991, p. 260), thus not only playing a crucial role in leading her herd, but transmitting her experience to her family. Over 20 years ago, Eisenberg wrote in a similar vein about female Asian elephants: The cow herd serves as a repository for traditional knowledge, including the routes to water holes during periods of drought, the routes to feeding grounds and so forth. Since the adult cows undoubtedly carry the memory of habitat utilization patterns, this is a form of living tradition (1981, p. 183). Female African elephants profound expression of affiliation reaches outside the immediate family unit to more distantly-related family members. Female elephants in the wild and in captivity have been repeatedly observed to engage in significant altruistic behavior, including allomothering. Estes (1991, p. 261) characterizes the degree of their expression of altruism as remarkable. Captive elephants also demonstrate such helping behaviors (Schulte 2000). Bonds between close relatives may be very strong and last a lifetime (Moss 1988). Subgroups of the same family, if reunited after a separation of only a few days, will greet each other with energy and excitement. Moss describes it this way: The two sub-groups of the family will run together, rumbling, trumpeting, and screaming, raise their heads, click their tusks together, entwine their trunks, flap their ears, spin around and back into each other, urinate and defecate, and generally show great excitement. A greeting such as this will sometimes last as long as ten minutes (1988, p. 128). Female elephants not only express affiliation with other subgroups of related family members, for example subgroups led by adult siblings, but also nurture social ties extending to bond groups composed of associated family units and clans and unrelated bond groups sharing the same range (Wittemyer et al. 2005). When contact occurs with related bond groups, bonds are renewed through greeting ceremonies of less intensity than those with close family members (Moss & Poole 1983). Over the course of their long lifespan and throughout their large home ranges, elephants come into contact with dozens of conspecifics and thus must acquire sufficient social skill to negotiate successfully the interactions with acquaintances, strangers and even enemies. The integrity of the elephants natal unit and complexity of its larger social world are critical to its life history. The natal herd protects the young and creates a social milieu in which the young elephant can mature and learn its role in adult life (Eisenberg 1981, p. 183). Female elephants in particular are socially gregarious animals capable of transmitting experience and knowledge to each other and engaging in altruistic behavior calculated to enhance the others survival. Female elephants experience of and need for affiliation is profound (Moss 1988).7
7. The details described in this section refer to savanna elephants. Less is known about forest elephants, a separate species. 256

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4.8 Physical vigor African and Asian elephants, all large, non-territorial herbivores, subsist in virtually any tropical and sub-tropical habitat providing adequate quantities of food and water. Elephants move through their home ranges throughout the year. Sukumar reports that female Asian elephant home ranges between 34 sq. km and 800 sq. km have been measured. The home range of a male Asian elephant was measured as ranging from 200-300 sq. km. Some home ranges appear to cover thousands of square kilometers. Eisenberg observed that Asian males move in a consistent home range, visiting various feeding and watering locations on a periodic schedule (Sukumar 2003). Home ranges for African family groups may vary from 50 to hundreds of square kilometers. African bull home ranges vary from 500 to 1500 sq. km (Shoshani 1997). African elephants travel 500-650 km during seasonal migrations (Langman, Roberts, Black, Maloiy et al. 1995, p. 629). Elephants range over 20-30 km on a daily basis in order to obtain sufficient food and visit dispersed sources of water (Shoshani 1992). Elephants space requirements are driven in part by their size. Equally important is their natural history. They are intensely social, physically powerful animals that have evolved to roam large tracts of land searching for water, foraging for food and minerals and exploring and investigating their physical environment. They also travel considerable distances in order to socialize with family, kin and other conspecifics. Elephants in the wild are typically on the move for 20 of every 24 hours. Of those 20 hours of activity, 18 are usually devoted to foraging. Eisenberg (1981) observed that Asian elephants stay in a single area for no more than three days before moving on. Accordingly, both African and Asian elephants require access to varied and appropriate habitat permitting them to engage in significant foraging behavior. Over time, elephants have evolved into creatures that can travel vast distances while expending relatively little energy (Langman et al. 1995). They are also capable of transforming the landscape, changing forest into savanna. A successful captive environment, therefore, must provide them with sufficient space to fully exercise both their endurance and strength. At this time, AZAs EMS mandates 75 sq. m of indoor space and 252 sq. m of outdoor space for two elephants. These mandates are unaffected by the climatic location of the exhibit (AZA 2003). In the wild, a modest elephant home range has been measured at 15 sq. km or 15,000,000 sq. m. It follows that AZAs permitted barn space is about 200,000 times smaller than the smallest known space female African elephants have chosen for themselves. AZAs outdoor space is roughly 60,000 times smaller than the smallest known elephant home range. AZA elephants frequent experience of arthritis, osteomyelitis and other chronic and sometimes fatal orthopedic disabilities is well known (Mikota, Sargent & Ranglack 1994; Csuti, Sargent & Beckert 2001; Fowler 2001; Roocroft & Oosterhuis 2001; Buckley, Chapter 14; Derby, Chapter 15; Mikota, Chapter 6). The health history of captive elephants in North America suggests that the act of traveling on a variety of substrates and terrain is important to maintain foot health in Asian elephants and to ward off arthritis and related disabilities and diseases in all elephant species (Fowler 2001).

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4.9 Optimal conditions of captivityHedigers perspective on the captive environment and Eisenbergs model of mammalian life strategies We do not assume that the only acceptable conditions of captivity are ones that closely replicate the complexity and scale of the wild. We do assume, however, that captive environmental options and opportunities must mimic conditions in the wild sufficiently to permit elephants to engage in their full repertoire of natural behaviors. The idea of employing knowledge of natural life histories in design and management of zoo animals is not new, but more often than not, its application is still novel. More than 50 years ago, Swiss zoo director Heini Hediger called for the development of zoo environments that provided for the behavioral, psychological and physiological needs of captive animals as deduced from the species natural history (1950, 1955). Much later, Eisenberg prepared detailed reports on studies of captive and wild mammals and developed a theoretical model based on life history strategies, which he described in his book, The Mammalian Radiations (1981). The ecological variables in Eisenbergs model offer a cogent means for assessing primary design considerations to match a zoo environment with a wild animals needs. Following Eisenbergs work (1981), zoo scientist Devra Kleiman made a breakthrough in the reproduction of the golden lion tamarin through studies of this and other species behavioral biology (1977). Similarly, John Seidensticker and James Doherty applied their knowledge of natural history to the behavioral management of zoo animals. They stated that the usefulness of behavioral studies in zoo exhibit design cannot be overemphasized and that significant exhibit improvements could not be achieved without reference to the natural history of the species (1996). At around the same time, one of us, with considerable help from her colleagues, offered a detailed model of zoo environmental analysis and design predicated on Hedigers (1950, 1955) andEisenbergs (1981) seminal works (Forthman, McManamon, Levi & Bruner 1995; Forthman 1998). 4.10 Delivering optimal conditions of captivity Consistent with Hedigers philosophy of providing the best care for captive animals by addressing an array of fundamental needs, Forthman and her colleagues proposed that zoos could provide optimal conditions of confinement informed by an animals natural history assessed in terms of discrete ecological variables, as identified by Eisenberg (1981). We believe this approach can and should be applied to elephants in captivity as well. They stated that the basis of animal management standards should be to provide optimal conditions in every aspect of our care of confined animals (Forthman et al. 1995; Forthman 1998, p. 237). In the 1995 paper, the essential aspects of captivity were assessed through a review and discussion of a largely theoretical literature. The 1998 paper, by comparison, described a comprehensive means to address many of those same variables with the applied goal of enhancing the quality of exhibitry and the care delivered. These two papers applied Eisenbergs model to define and describe components of optimal care, first for mammals generally and then specifically for ungulates in captivity. The papers provide a theoretical and applied discussion and analysis of each variable, but because the second paper focuses on ungulates we will use that paper primarily to summarize the main points, and to describe research on behavioral and ecological variables first identified by Eisenberg. Also, using that paper as a base reference we extrapolate the significance of the variables from ungulates to captive elephants.

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4.11 Definitions Physical variables: These factors include geographic range, body size and life history strategy. Sensory variables: These factors include visual, auditory, tactile and olfactory environmental stimuli. Occupational variables: These factors fall into two broad categories: activity cycle and habitat use. Feeding variables: Two significant feeding variables cross both occupational categories: foraging strategy and diet. Social variables: This ecological category has the longest list of critical elements, including social structure, reproductive behavior and vulnerability of the species young. 4.12 Physical variables Geographic range The term geographic range encompasses, in gross terms, the physical limits over which an entire species carries out its natural life cycle. Geographic range encompasses all habitats to which a species is adapted (Eisenberg 1981). For example, savanna elephants are found in temperate woodland, savanna, riverine forest, bush, desert, etc. We argue that geographic range is important precisely because its implications are frequently ignored by the zoo community (Forthman 1998, p. 238), and we recognize that the ability of humans to provide for captive animals is constrained, at best. As one example, stress is commonly caused by the failure of captive conditions to provide the subject animals with the environmental options necessary to permit them to exercise evolved thermoregulatory strategies: When thermoregulation begins to constrain other species-specific activities, the animal is both deprived and distressed (Forthman 1998, p. 238). This problem carries further implications with respect to body size. Body size Body size is closely related to geographic or home range size. Typically, the larger the mammal, the larger the home range. Principles of allometry or scaling are important not only in the understanding of morphology and physiology but also in behavior (Schmidt-Neilsen 1972; Calder 1984; Owen-Smith 1988). Allometry dictates that animals at either end of the body size distribution will be most subject to thermal stress. Because elephants are the largest extant land mammals, attention to their thermoregulatory needs is critical to their humane housing and exhibitry. Langman and his colleagues (1990; Langman, Rowe, Forthman, Whitton et al. 1996) have studied the implications of zoo exhibit materials on thermoregulation and thermal stress in zoo animals. In studies with elephants and sea lions, for example, they have shown that gunite, which has dangerous thermal properties but is the zoo industry standard for artificial rock, can put animals at risk of significant thermal distress. Further, in studies with wild rhino and zoo elephants, they report that both species are obligatory heterotherms that store heat in their body tissues when temperatures exceed 23C (74F). They caution that unless elephants are able to dump stored heat into the cool night atmosphere, they may be subject to chronic thermal stress (Langman 1985; Langman, Rowe,
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Forthman; Langman et al. 2003) and the health problems this may promote (Sampson 1999).8 Most elephants are held at night in enclosed structures, thus preventing this natural process. Allometry also affects elephants kept in cold climates. Because a form that has a small surface-area-to-volume ratio heats slowly, elephants subjected to consistent cold temperatures suffer the converse effects, being unable to gain sufficient heat to warm themselves, and their extremities in particular. Recent research indicates that the thermal equilibrium of captive elephants is more closely correlated to environmental radiation than to air temperature alone (Rowe, Langman, Bakken, Forthman et al. in prep.).Current AZA elephant management guidelines recommend bringing elephants indoors at 40F, but thermal energy exchange for an elephant at 40F on a sunny day is quite different than 40F on a cloudy day. Inter- and intra-species variation in elephants ability to respond behaviorally and physiologically to thermal extremes may exist due to differences in size, anatomy, and thermal acclimatization. Therefore a thermal index for management of elephants exposed to cold temperatures should be based not just on temperature but on the elephants size and existing environmental radiation (Rowe in prep.). Accordingly, we believe that exhibit materials should approximate the thermal characteristics of earth and rock, as hollow gunite forms do not absorb heat (or cold). Further, species-appropriate water or mud features as well as multiple opportunities for shelter must be provided to produce the microclimates animals seek in nature (Langman et al. 2003). Shelters are defined as structures that go beyond simple shelter from the sun in those climates in which the heat index (a measure of apparent temperature that takes into account relative humidity) may be very high (Forthman 1998). One rule of thumb suggested is to create multiple areas in each exhibit that provide four thermoregulatory options: sun and wind, shade and wind, sun with no wind and shade with no wind (Langman et al. 2003). Consideration of the heat index is important, especially for large mammals at risk of hyperthermia (Forthman et al. 1995). For example, shade may be insufficient to offer an effective thermoregulatory option if the heat index in the shaded area is higher than in direct sun, due to poor air circulation or higher relative humidity. Accordingly, shade alone is not a sufficient thermoregulatory option for large mammals that need to reduce their thermal loads (Langman 1985, 1990). Field research on thermoregulation indicates that in the wild each species uses behavioral options to maintain a balance between heat gain and loss (Langman et al. 1996). They report that evaporation only accounts for 20-30 percent of total heat loss; behavioral thermoregulation is the most important thermoregulatory strategy for most species. They observe that captive enclosures rarely provide a species with a range of behavioral choices as large or as diverse as those in the wild. Recognizing that ambient conditions in an exhibit during the summer months may exceed the upper critical temperatures for a species (in this case, sea lions: Langman et al. 1996) they suggested an alternate indoor habitat, cooled to temperatures below the published upper critical temperature. Life history strategy Body size also relates to life history strategy (Calder 1984), in that longevity is positively correlated with body size. Ungulates are herbivores, and they generally live longer than omnivores or carnivores of equal size. Further, because most large ungulates have small litter sizes, the death of even one offspring is significant to the animals reproductive fitness, and is relevant to any attempts
8. From a veterinary perspective, chronic or intermittent stress has a potentially harmful effect on all aspects of animal health (Baer 1998, p. 279). Chronic or intermittent stress has been associated with impaired reproduction (Moberg 1985), increased susceptibility to disease (Landi, Drieder, Lang & Bullock 1982), gastric ulcers, cardiovascular pathology and alterations in basal metabolism (Klasig 1985). 260

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to propagate captive species (Eisenberg 1981). This fact implies that providing optimal captive environments and care for many ungulate species is a long-term proposition (Forthman 1998, p. 239). A review of these variables leads to the conclusion that facilities for ungulates must be designed to accommodate individuals throughout their lives. While maintaining fundamental features that contribute to the ungulates sense of security, both in a familiar home range and with respect to refuges that protect immature or low-status animals from aggression, interference or environmental extremes, temporal variation of enrichment objects is important to approximate the complexity of their natural environment. Further, relatively stable social groups should be maintained over time to best approximate field conditions for most social species, including continuity of care-taking staff (Forthman 1998, p. 239). 4.13 Physical variables and elephants Elephants need for space is not only driven by their body size but also by their key characteristics as highly social, physically vigorous individuals. Elephants need for space is also a function of the species natural history playing out in a warm climate over large tracts of land. See additional discussion of the topic in the section on Physical vigor. As stated previously, body size and longevity are positively correlated. It is not surprising, therefore, to consider that Asian elephants have a lifespan of roughly 50-70 years and Africans a potential lifespan of 80 years (Walker 1975). Accounting for this potential places a heavy burden on zoos to develop appropriate lifespan planning. Such planning would address, at a minimum, the needs of aging, sick and disabled elephants (Maple 2003). It is incumbent on zoos exhibiting elephants to develop and maintain technical expertise in the diagnosis and delivery of geriatric care, to provide remedial environmental options both indoors and outdoors to protect vulnerable animals and to develop standards that keep elephants healthy and comfortable for the longest possible period of time. It is equally essential that zoos continue to provide for the welfare of zoo elephants by retiring them to appropriate facilities when their resident institution cannot address or ameliorate their health condition (e.g., arthritis, chronic foot disease, lack of social companions, unabated stereotypic behaviors or other significant disability) or can no longer exhibit them effectively and humanely (Buckley, Chapter 14; Derby, Chapter 15). 4.14 Sensory variables Elephants have formidable senses of hearing (e.g., Payne 1998) and smell (Poole & Moss 1981; Poole 1987; Lazar, Rasmussen, Greenwood, Bang et al. 2004; Poole & Granli, Chapter 1). Elephants also have an acute tactile sense that is equally important for social communication. Because captive mammals perception may not always be the same as that of the humans who design their facilities or who provide care for them, sensory over-stimulation, or the masking of species-specific cues by irrelevant or distressful ones, must be considered as a potential and often subtle source of distress (Forthman et al. 1995; Forthman 1998, p. 240). Vision Light or illumination is a critical environmental variable to consider when designing captive mammal facilities. Few studies have attempted to quantify the deleterious effects of improper lightingwhether too much or too littleand the effect on species held indoors for long periods (e.g., Helfman 1981).

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Audition Audition serves many critical functions for elephants (Payne 1998). Forthman (1998, p. 240-241) observes that, Certain conditions associated with confinement may subject ungulates to auditory distress, chronic or acute, predictable or random (Hanson, Larson & Snowdon 1976; Peterson 1980; Gamble 1982; de Boer, Slangen & van der Gugten 1988; de Boer, van der Gugten & Slangen 1989; Thomas, Kastelein & Awbrey 1990; Gold & Ogden 1991). Because of the nature and function of elephants range of auditory sensitivity, they may be especially sensitive to mechanical sounds. Deleterious physiological and behavioral effects of loud noise are well documented (Peterson 1980; Stoskopf 1983; Krause 1989; Thomas et al. 1990). Frequency of sound also profoundly influences the psychoneuroendocrine and immune systems of animals (Forthman et al. 1995). We recommend that decibel level and frequency of irrelevant noise, particularly in the elephants holding areas, should at the least be kept at a minimum. See additional discussion of audition under cognitive ability and social complexity. Olfaction Necessary cleaning and disinfecting of exhibits and holding areas can deprive captive mammals of olfactory stimuli, including urine, feces and glandular secretions, even though such stimuli provide a vital function in spatial orientation and social communication (Forthman 1998, p. 241). 4.15 Sensory variables and elephants Many holding areas for elephants are constructed of acoustically reflective concrete (see Buckley, Chapter 14, for an alternative). This is another reason arguing in favor of the pragmatic advantage of holding elephants in a climate to which they are suited. While the provision of veterinary care and husbandry might require holding areas, a suitable climate would minimize the amount of time an elephant would spend in enclosed areas. Zoo elephants access year round to quiet (but not acoustically dead) space outdoors as well as indoors may be critical, given the importance of sound as an environmental variable and elephants broad use of auditory signals for communication. Similarly, the preservation of olfactory stimuli could be enhanced when elephants are exhibited in climates similar to those in which they have evolved. This would result in less time spent confined to sanitized holding areas. To the extent that spacious exhibits more appropriate to the size of elephants and their home ranges are constructed, rotation of pastures could reduce the necessity for constant removal of solid waste. Research reported in the August 2004 issue of Chemistry and Biology discusses pheromone transport in Asian elephants (Lazar et al. 2004). The investigation reported that female Asian elephants communicate their readiness to mate by excreting a sex pheromone in their urine. Males detecting the pheromone touch the pheromone-loaded urine with their trunk tip and then place some of the urine in their mouths, for analysis in the vomeronasal organ, after which mating typically ensues. The importance of chemical signals in reproduction has also been documented among African elephants (Poole & Moss 1981; Poole 1987). In those zoos that insist on reproducing elephants, exhibit construction and social groupings of individuals should take heed of this information about the important role that olfactory stimulation plays in elephant reproductive strategy.

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4.16 Occupational variables Activity cycles Observations of ungulates and elephants suggest that they are polycyclic (Eisenberg 1981; Moss 1988). This activity pattern results from the interaction of feeding, thermoregulatory behavior and, to a lesser extent for elephants, anti-predator strategies (Eisenberg 1981; Moss 1988). Consequently, the provision of optimal care requires work shifts and sufficient security precautions to permit animals to remain outdoors for the majority of the time, except when caregivers bring the animals in periodically each day for brief monitoring. Habitat use Habitat use is inextricably bound to feeding strategy. It is well known that African elephants tend to exploit relatively open habitat while Asian elephants are usually found in more heavily wooded environments (Moss 1988; Sukumar 1994). Yet most large herbivorous mammals are confined by zoos to monotonous exhibits in which the animals are managed on compacted dirt, perhaps enhanced with a mud wallow and small patches of hardy or heavily protected vegetation (Forthman 1998, p. 242). These observations are especially relevant to many zoo elephant exhibits. An aggressive redesign of exhibits holding large ungulates is necessary: It is imperative to provide access for trucks, cranes and other heavy equipment necessary to install and replace large exhibit furnishings, including entire trees, as well as to till compacted substrates, add gravel and replant or reseed. Plans for adequate irrigation and careful selection of the hardiest grasses and herbs are also extremely important in the maintenance of vegetation. Surface area, terrain, and substrate are additional considerations in designing and maintaining habitats that will elicit species-typical behaviors (Forthman 1998, p. 242). 4.17 Occupational variables and elephants Elephants in the wild occupy approximately 18 hours of their day browsing or grazing. They move almost continuously while feeding. The remainder of their day is largely given over to socializing, water or dustbathing or wallowing in mud. They rest for approximately four hours a day (Eisenberg 1981; Moss 1988). Given the manner and duration of activity of elephants in the wild, options must be available to captive elephants that allow them to maintain a normal activity pattern (Hancocks, Chapter 17). Options basic to elephant occupational variables would include room to roam on a variety of substrates, with a variation in topography, and access to appropriate plant material or large and free provision of cut fresh browse (branches) for species-specific foraging (Kinzley, Chapter 12). Other basic occupational options suggested by elephants natural history include daily access to dust, water and mud of sufficient volume to permit totally submerged bathing and all-body wallowing. 4.18 Feeding variables Foraging strategy and diet How an animal forages influences more than its diet. Foraging strategy influences ranging patterns, activity budgets, and social organization (Forthman 1998, p. 242). Grazers typically spend more time foraging than browsers, due to the relative nutritional quality of the forage (Eisenberg 1981).
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When a species has evolved to perform a linked set of responses, in this case forage and then feed, they adapt with difficulty to disruptions in that linkage (Forthman et al. 1995). When a normal consummatory response is delayed or prevented, maladaptive behaviors are often performed. Animals exhibit these maladaptive behaviors to reduce potentially damaging physiological stress responses. Arbitrary feeding schedules cause animals like ungulates to suffer from this dissociation of appetitive and consummatory behaviors. Such dissociation can result in vacuum behaviors during feeding (e.g., fence-licking by giraffes deprived of leafy branches) and locomotion, such as weaving and pacing among species that normally range widely. Adequate amounts, distribution and availability of appropriate plant material, especially if available at an early age, can prevent these problems from developing. Diet selection requires learning. Ungulates must learn to select from a vast number of plants, choosing those parts that are most nutritious and avoiding those that contain harmful amounts of toxins. Visual, olfactory and gustatory cues, together with time and experience, all play a role in the ungulates process of learning to select an appropriate diet. The arbitrary provision of processed food, pristine hay and fresh fruits and vegetables in a monotonous exhibit or holding area does not permit the animal to engage the full range of its abilities and behavioral repertoire (Swaisgood, Ellis, Forthman and Shepardson 2003; see Forthman 1998, p. 243-244 for review). 4.19 Feeding variables and elephants Elephants are adapted in the wild to range over large areas and to forage for a considerable part of any 24-hour period (Poole & Granli, Chapter 1). Elephants represent the ultimate adaptation for feeding upon coarse plant materials (Eisenberg 1981, p. 183). An elephants teeth are highly adapted for grinding down tough grasses, sedges and bark. Because it is adapted for feeding on plant materials with relatively low nutrient content, [f ]eeding may occupy from 70 to 80 percent of an elephants waking hours, and in the process of selective feeding it may consume 250 to 400 pounds of wet forage in an average twenty-four-hour period (Eisenberg 1981, p. 183). Elephants feed night and day. While Asian elephants take in a significant amount of grasses, for females and young especially, branch-feeding in the forest occupies 30 to 50 percent of their feeding time (Eisenberg 1981, p. 184). Foraging and diet are key elements of an elephants occupation cycles (Eisenberg 1981; Moss 1983; Sukumar 2003). There are significant gaps, however, in our understanding of elephants diets, in particular. For example, recent field research indicates that termite mound soils, which contain higher concentrations of calcium, magnesium, potassium, sodium and phosphorus, support plants and trees subject to more intense feeding by African elephants than plant material from the surrounding area (Holdo & McDowell 2004). Earlier research suggests that elephants ingest termite mound soils, possibly as a mineral supplement to their diet (Ruggiero & Fay 1994). Accordingly, termite mounds may play an important role in determining food availability, dietary mineral intake and spatial feeding patterns by elephants, as well as ranging perhaps, as termite distribution is limited by altitude. Still, we know that elephants spend more time foraging and feeding than any other activity (Owen-Smith 1988). Further, foraging and feeding among elephants requires considerable learning (Lee & Moss 1999). The absence of appropriate opportunity to engage in foraging and feeding can result in stress to the animal (above). In most zoos, elephants lack control over access to appropriate food sources. Accordingly, it is incumbent on those keeping captive elephants to deliver a species-appropriate diet in ways that permit species-specific foraging strategies that address the full range of their dietary needs
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and avoid creating new health and behavioral problems. The provision of ample volumes of fresh browse material (branches) is especially critical (Stoinski, Daniel & Maple 2000; Kinzley, Chapter 12). 4.20 Social variables Appropriate social groupings can lead to dramatically improved propagation of the species (Clubb & Mason 2002). The principal problem associated with confining large, socially gregarious animals such as elephants, is the inability of most zoos to provide appropriate space for a sociallyviable-sized group. We believe one solution to this problem is obvious: If insufficient space is available for an appropriate herd, the species should be excluded from the collection (Forthman 1998, p. 244). Reproductive behavior and social context Even in confinement, highly social animals raised by their mothers in adequate space and appropriate social groups, typically develop normally (Bloomsmith, Pazol & Alford 1994; Maple et al., Chapter 10). The powerful role of social relationships to the health of individual elephants makes it imperative that captive female elephants intended for breeding be given the social context in which to undertake the task of delivering and raising a calf, a task that will require zoos to meet far higher standards of space and management than are typical today. Elephant reproduction9 must also take into account the probability of surplus males. Formation of single-sex groups, like bachelor herds, may be appropriate in facilities with adequate space (Forthman 1998); this has been shown to be possible with gorillas (Stoinski, Kuhar, Lukas & Maple 2004). Vulnerability of young Vulnerability of young in confined settings usually results from disease or intra-species aggression and relates to management of space and group composition. Age at weaning and emigration from the herd must be considered and planned in advance as well. It may be optimal to maintain a stable female group in an exhibit over time and to exchange breeding males (Forthman 1998, p. 246). Research demonstrates the persistent influences of early environmental experience on neural organization (e.g., Bradshaw, Chapter 4). It follows, therefore, that exhibits, indoor and outdoor enclosures and corrals must be designed to accommodate the several distinct developmental stages and special vulnerability of elephant youngsters. Exhibit designs and staff skills facilitating the provision of a natural, complex and varied captive environment are probably key in production of behaviorally flexible, fit, and competent animals