REVIEW: ELEPHANTS CONCEPTS IN CARE AND WELFARE IN CAPTIVITY 63

Int. Zoo Yb. (2006) 40: 63–79 © The Zoological Society of London

Concepts in the care and welfare of captive elephants J. VEASEY Woburn Safari Park, Woburn, Bedfordshire MK17 9QN, United Kingdom E-mail: [email protected]

Zoos are duty bound to maintain a high standard of challenges facing zoos both from an welfare for all animals for which they are respons- ible. For elephants, this represents a greater chal- animal husbandry and a public perception lenge than for many other species; their sheer size, perspective. This document is not sophisticated social life, high level of intelligence and designed to be a formula for elephant wel- large behavioural repertoire, combined with their fare in captivity because there are still too origins in tropical and subtropical climates mean that replicating the physical, social and environ- many un-answered questions, rather it is mental requirements needed for a high standard of intended as a discussion of some of the welfare in captivity is a significant challenge. This is concepts relating to captive elephant wel- compounded by the difficulties in measuring welfare generally, and specifically for animals such as ele- fare, which it is hoped, might encourage phants within zoo environments. Evidence does exist people from a variety of viewpoints to relating to the longevity, reproductive success and consider elephant welfare in a different the health status of captive elephants which suggests way. I will not go into the issue of whether that their management is not at as high a standard as it is for many other species kept in zoos, and that or not elephants should be in captivity elephant welfare is likely to be compromised as a because this would be a not inconsider- result. It is suggested that for as long as elephants able document in its own right, but I will remain in captivity that their management should be based around the requirements of the animals them- work on the assumption that whilst ele- selves taking into account an understanding of their phants are in zoos, elephant holders are biology and behavioural ecology. Given the difficul- duty bound, as they are with all other ties in measuring welfare, it is suggested that those species, to optimize the welfare of these responsible for elephant management should not rely on proof of suffering prior to making adjustments animals without unduly compromising to their programmes, but in the first instance con- appropriate conservation and educational sider the likely physical and behavioural needs of the aspirations for the herds. With this in elephant. As a minimum, facilities should provide for those behaviours and contingencies which are bio- mind, I will attempt to explain what wel- logically significant in terms of survival and repro- fare is and what it is not, and how it is duction in the wild, which take up a significant measured. I will then give my personal proportion of an elephant’s time in the wild and are not necessarily triggered by external stimuli alone. It opinion on why the management of ele- is suggested that a high standard of captive elephant phant welfare in captivity is a challenge welfare is theoretically attainable and that significant and provide some suggestions of how zoos improvements in welfare are likely to be achieved by might overcome these challenges in the addressing inadequacies in the physical environment which predispose captive elephants to trauma and by future. As will become apparent, there is providing for appropriate social and foraging a dearth of ‘facts’ when it comes to the opportunities. issue of captive elephant welfare, and as a Key-words: digestive strategies, elephant care, ele- result, what I present here, is very much a phant welfare, facilities, guidelines, health, hus- personal opinion, but one I hope that is bandry, management, social groups, standards, zoos as objective as possible, and one for which, I give elephants the benefit of any The welfare of elephants in captivity is doubt I may have when hard evidence is perhaps one of the greatest management lacking. 64 ELEPHANTS AND RHINOCEROS

WHAT DO WE MEAN BY WELFARE? welfare (see Fraser & Broom, 1990). Animal welfare relates specifically to an Whilst it is clear that reduced welfare can animal’s state of psychological wellbeing, decrease reproductive output and genetic in other words what it feels, rather than fitness (Archer, 1979), this is not always what it does. In practical terms, one might the case, it would be incorrect for example consider good welfare to be a state in to assume intensively managed livestock which an animal experiences positive emo- benefit from their markedly increased tional states and an absence of suffering. reproductive output over and above wild However, because an individual’s experi- relatives or to assume that their welfare is ences, thoughts and feelings are largely definitively acceptable just because they inaccessible, particularly in the absence of are reproducing. a common language, we are reliant upon In the same way that health, reproduc- indirect indicators of an animals’ mental tion and welfare are not equivalent, death state and hence its welfare. As a result, also has to be differentiated from welfare what are commonly referred to as welfare because death can effectively be defined measures, are in fact welfare indicators, by the cessation of brain activity, and wel- and none should be considered as reliable fare is essentially a function of brain in isolation as will hopefully become activity. However, this does not prevent apparent. death being an ethical issue, and by ethical Having very briefly defined what wel- I mean relating to prevailing moral stan- fare is, it is equally important to under- dards, nor does it mean that the causes of stand what welfare is not. Although the death are inevitably without a welfare health status of an animal can affect its dimension. How an animal dies, and what welfare, and the welfare of an animal can factors precipitated its death; whether it affect its health, health and welfare are was caused by inadequate care or resulted distinguishable. Health refers to the in suffering, etc, must be considered as rel- physical rather than the psychological evant to a welfare discussion. wellbeing of an animal and so, if a disease causes pain, reduces mobility or the HOW DO WE MEASURE WELFARE? ability of the animal to interact with con- If we accept that welfare is a measure of specifics it may reduce the individuals’ an animals’ mental wellbeing, how is this welfare but an ailment that does not (yet) measured? Like the challenge zoos face in impact upon the behaviour or pain recep- managing elephant welfare, the challenges tors of the animal, may not necessarily scientists face in assessing animal welfare impact upon welfare at that time. One is also a considerable one (see Mason & such example of this might be an intra- Mendl, 1993). The methods of assessing cerebral aneurysm where a weakness in welfare can be grouped into three broad blood vessels within the brain has no categories, those that involve measuring impact on welfare until such a point that behavioural and physiological responses the aneurysm bursts killing the individual to stressors which reflect the animal’s concerned. Thus an individual possessing mental state, and those that involve meas- such a defect must be considered to be in uring variables external to the animal that poor health, without actually suffering as we might reasonably assume will affect a result of the defect, unless health itself the animals’ mental state and correlate is defined in such a way as incorporates a with, or indeed cause reduced welfare in welfare component. It should be noted the species concerned. Rarely are these that this view is contrary to some who techniques used in isolation, and variables relate genetic fitness (that is to say, the that may precipitate poor welfare, such as extent to which an individual is able to certain aspects of the animals’ physical or increase the frequency of its genotype) to social environment, can be mitigated by REVIEW: ELEPHANTS CONCEPTS IN CARE AND WELFARE IN CAPTIVITY 65 management practices for example, such may activate an acute ‘stress’ response, that welfare standards can be upheld. As potentially invalidating any worthwhile a result, every measure has to be con- conclusions. In situations of chronic sidered in a broader context. stress, the HPA response can also be Both behavioural and physiological depressed. It should also be noted that in responses to the suboptimal circumstances the UK at least, invasive procedures such that reduce welfare are typically what we as ‘experimental blood sampling’ are would view as adaptive in that they rep- likely to require approval from govern- resent attempts made by the animal to mental agencies. improve its welfare by coping with, or If the ‘stress response’ is not successful eliminating stressors, although in cases of in eliminating the stressor, long-term chronic stress, the prolonged activation of activation can ultimately reduce the health short-term coping responses may not of the individual, and these chronic appear adaptive. The greater the animal is physiological stress responses can also be required to cope, or indeed the greater the measured. These include immunosuppres- animal is motivated to avoid or escape the sion, reduced fecundity, reduction in pro- stressor, the more its welfare is likely to tein synthesis (body-mass loss), elevated be compromised, and the greater the blood pressure, ulceration, thickening of coping response that is likely to become the arteries, premature death, etc. These manifest. As a result, the magnitude of the chronic stress reactions may be parti- animals’ response will give an insight into cularly useful in assessing the level of the degree to which its welfare is everyday welfare of zoo animals because compromised. they should reflect welfare status under the prevailing conditions rather than the PHYSIOLOGICAL MEASURES animals’ state of mind at the point of Physiological responses to stress are com- measurement. However, there are prob- plex, multifaceted and vary according to lems with these measures; firstly, these the nature of the stressor. In the crudest chronic stress indicators are difficult to terms, the stress response is characterized measure in live animals, secondly, it is by an elevation in glucocorticoids secreted very difficult to determine what caused the by the hypothalamic-pituitary-adrenal reduction in welfare that resulted in these (HPA) axis (Carlstead & Brown, 2005). changes. The secretion of these steroid hormones facilitates the mobilization of energy BEHAVIOURAL MEASURES reserves and an acceleration of cardio- Largely as a result of the problems pre- vascular tone to prepare the animal for a viously outlined, behavioural studies are a coping response; fight or flight. popular approach to welfare assessment, Physiological welfare indicators pri- particularly in non experimental condi- marily involve measuring the compounds tions such as those in zoos. released by the animal in its blood, and to a lesser extent in excreta and saliva when Time budgets and comparisons with the these systems are activated, and also wild Time budgets are essentially behav- short-term changes in rates of respiration, ioural measures of how animals allocate etc. These measures have to be treated their time. Captive time budgets can be with caution because an elevation in glu- used as a baseline against which to assess cocorticoids can be activated in a manner the affects on behaviour of changes in comparable to a ‘stress response’ when an management, or in the animals’ physical animal is excited or has exerted itself, and and social environment. Time budgets indeed the sampling procedure itself, from wild animals can also be used to particularly if this involves taking blood, indicate areas of possible concern in cap- 66 ELEPHANTS AND RHINOCEROS tive animals, in fact, some have argued The strength of preferences can be that merely demonstrating a difference measured by applying Consumer Demand between wild and captive behaviour is Theory and making the animal give up sufficient to assume a reduction in welfare resources; sacrificing food, comfort (Thorpe, 1965, 1967; Martin, 1979), or resources and social contact or working to that there is an inherent welfare value in gain access to their preferences; pressing the state of wildness (Wuichet & Norton, levers, swimming through cold water, 1995), notwithstanding the welfare chal- pushing open heavy doors, etc. The lenges regularly experienced by wild harder the animal is prepared to work or animals over and above those experienced the more it is willing to sacrifice, the by most zoo animals, such as predation greater the preference, and as a result the and risk of predation, territorial aggres- greater the likely welfare compromise if sion, disease, injury, starvation, climatic denied access to that resource/oppor- extremes, etc. In reality, there should be tunity. Such an approach in giving an measurable welfare consequences, or insight into the relative preference for cer- additional evidence prior to making ‘wel- tain resources can be used to assist in fare judgements’ between qualitative and facility design and can also give an insight quantitative differences in behaviour into the relative importance of behav- between wild and captive conspecifics ioural variables because animals can be (Veasey et al., 1996a). However, an made to work to perform certain behav- absence of proof of suffering cannot be iours such as ‘working’ to gain access to viewed as a proof of an absence of suf- conspecifics with which to groom, mate or fering, and as a result, it may be reason- interact with, or features needed to trigger able to take a precautionary approach to specific behaviours, such as rubbing posts, welfare in certain circumstances as I hope dust bathing sites or pools, etc. will become clear. Evolution will have led to behaviours of a high survival or reproductive value Behavioural needs and preference being rewarding to perform and/or make tests Animals can also provide an the animal highly motivated to perform insight into their welfare by expressing them, and so it is not unreasonable to preferences for certain variables. Prefer- assume, that denying animals the oppor- ence tests have been used to indicate what tunity to perform these behaviours may animals like, chickens have for example have welfare consequences. The degree to been shown to prefer larger cages with a which an animal is motivated to perform substrate to smaller cages with a wire specific behaviours can be assessed experi- floor (Dawkins, 1983), which would mentally (see Dawkins, 1983) but can also appear to suggest that chickens denied be informally assessed in non-experi- access to space and a substrate may have mental situations. For example, elephants impoverished welfare. However, there are which sacrifice feeding opportunities to of course limitations; firstly preference spend time in close proximity to confined tests only indicate a relative preference members of the herd are suggesting a not a measure of the strength of a pref- relative preference for social contact at erence, secondly simply because an animal that time and as such we might reasonably expresses a preference for a certain vari- assume that companionship is potentially able, does not mean it will inevitably an important component of the welfare of suffer in its absence, and lastly animals do that individual. not always make choices that are in their When animals demonstrate a willing- best interests as can be most clearly under- ness to sacrifice resources or work hard to stood in the selection of diet and exercise express particular behaviours, it is more regimes. likely that these will qualify as ‘behav- REVIEW: ELEPHANTS CONCEPTS IN CARE AND WELFARE IN CAPTIVITY 67 ioural needs’ and we can reasonably ranging conditions, or to which that assume animals are likely to suffer if animal appears highly adapted and or denied the opportunity to express them. motivated, then husbandry and housing Behavioural needs are essentially behav- practices should accommodate for this in iours that animals must perform for their captivity wherever possible. With behav- welfare to be satisfied. Other than being iours or environmental factors that fall behaviours animals will often work for to into these categories, it is best to take a perform, behavioural needs are typically precautionary approach and rely on proof behaviours of high survival or reproduc- that the absence of these elements does tive value, potentially of a long duration, not cause suffering before dispensing with energetically demanding and often inter- them rather than relying on proof that nally stimulated (that is to say not neces- their absence does cause suffering. sarily reliant upon triggers external to the animal). For example, given time, many Abnormal behaviours Behavioural meas- species will become motivated to forage ures of welfare can also centre on the fre- even when food stimuli are not present or quency and duration of ‘abnormal’ when they are nutritionally sated, but behaviours, the most obvious of which are predator escape behaviour, although of stereotypic behaviours. These unvarying high survival value, is not considered as a and apparently pointless behaviours behavioural need because it need only be (Mason, 1991a) do not necessarily cause exhibited in the presence of the appro- reduced welfare but have been linked to priate external stimuli, namely the pred- poor welfare as they are typically seen in ator or the perception of a predator. An animals for which we might assume wel- animal given the opportunity to feed for fare to be low, such as those in barren or 2 hours in captivity may be satisfied in small environments, those suffering pain terms of nutritive requirements, but with or distress and those in which other wel- regards to behavioural requirements, if fare correlates are manifest, such as those they typically graze or forage for with injuries or obvious social stressors, 14–20 hours per day in the wild, they may etc. However, stereotypies must also be well possess a ‘need’ to feed/forage more treated with some caution, because they extensively and so may suffer if the void can also occur when an animal is excited left in their time budget is not appro- as well as when stressed (Veasey, 1993), priately filled. In examples such as this, furthermore, it is believed that stereotypic where the difference in time budget is so behaviours may be satisfying to perform substantial, one has to consider, how such in that they resemble frustrated behav- a large differential for such an important iours or by providing a regular control- behaviour could realistically be compen- lable level of stimulation that helps the sated for in captivity in any other way animal cope with unpleasant or uncon- without there being welfare consequences. trollable neural stimulation. Thus stereo- In reality, proof of either negative or typic animals often have lower heart rates, insignificant welfare consequences for the higher levels of circulating endogenous non-expression of wild behaviours may opiods and reduced cortisol levels in com- not be attainable, and so I would suggest parison to non-stereotypic animals in the following approach. Where an animal similar conditions (Dantzer, 1986; Mason, has evolved to perform a specific behav- 1991a). Thus although it can be argued, iour or live in a particular social or that whilst stereotyping, animals may not physical environment, which would necessarily be suffering per se, it can also appear to be of high survival value, tend be argued, that the presence of stereoty- to take up a significant proportion of that pies indicates the animal has been animals’ time or energy under free- required to perform a coping response 68 ELEPHANTS AND RHINOCEROS and as such has experienced a welfare stressors, lack of behavioural or social challenge (not withstanding stereotypies opportunities, the restriction of feed, lack induced by excitement/anticipation, etc). of choice and control, etc. These corre- One further additional factor compli- lates can be adapted for different species cating the relationship between stereoty- when combined with an understanding of pies and welfare is the fact that even once their behavioural ecology. Thus we might conditions have been improved, stereoty- reasonably assume a lack of social inter- pies can persist (Mason, 1991b) and so action is likely to be a greater issue for a may not reflect the prevailing conditions social primate, such as a Chimpanzee Pan the animal is subject to. This may be troglodytes, than it would be for a solitary particularly true for elephants in zoos predator, such as a Tiger Panthera tigris, because they often have complex and and we might also be forgiven for varied life histories which may include assuming that the compression of an ele- periods in which stereotypies might phant’s extensive daily foraging routine develop and experience has shown that into 2–3 hours in captivity might pose a even once elephants have been removed greater welfare challenge than altering a from these conditions, stereotypic behav- snake’s feeding ecology in captivity iours often persist. Furthermore, it should because it takes up a much less significant also be noted that behaviours classified as proportion of its time in the wild. How- abnormal in captivity, such as certain ster- ever, caution is of course required, and eotypic behaviours, have been described now is perhaps the time to reiterate, no in wild animals (Veasey et al., 1996b) single variable is satisfactory on its own. though on generally on a far less frequent External welfare correlates are a key basis. component of the Five Freedoms which Other ‘abnormal’ behavioural indica- were developed to help simplify welfare tors often linked to welfare might at first concepts in order to facilitate the provi- appear more straightforward, these may sioning of adequate welfare standards, include excessive signs of distress (vocal- particularly for agricultural animals. izing, extreme timidity or aggression, These freedoms included the (1) freedom escape behaviours, etc), self mutilation from injury and disease, (2) freedom from and reduced performance of behaviours hunger, thirst and malnutrition, critical to survival and reproduction, such (3) freedom from thermal or physical dis- as grooming, mating, foraging/feeding, tress, (4) freedom to express most etc. However, once again, the context of ‘normal’ behaviours and (5) freedom these behaviours needs to be carefully from fear. It is felt that by providing for considered when attempting to attribute a these freedoms, welfare will be assured, cause for these behaviours. and although developed for agriculture, these are incorporated into the UK zoo ENVIRONMENTAL WELFARE CORRELATES licensing legislation (DETR, 2000). This final set of welfare indicators are Although the five freedoms are not strictly external to the animal. They are factors a framework for measuring welfare, they that based on a number of studies have are useful in giving structure and context proven to be correlated with other welfare to captive animal welfare. indicators, and for which, we can intui- tively see a link between their existence CARTESIAN THEORY AND THE PRINCIPLE and a reduction in welfare. Such factors, OF PARSIMONY which are commonly associated with indi- This very brief introduction into the cators of reduced welfare, include small, measurement of animal welfare highlights barren environments and or the restriction its comparative uniqueness amongst other of the animals’ movement, uncontrollable scientific disciplines, in that definitive REVIEW: ELEPHANTS CONCEPTS IN CARE AND WELFARE IN CAPTIVITY 69 proof is unlikely to be attainable in most further argues that just as humans can cases. I will now briefly introduce two respond to stimuli in an unconscious way, more concepts which have had a major in other words we can act without feeling bearing on animal welfare science and the or thinking, it is argued that an animal interpretation of data. need not experience pain to avoid what we The first is the ‘principle of parsimony’ would view as painful stimuli, and that (also known as Occam’s razor) whereby just because we feel pain, it does not mean one applies the simplest explanation or to say that an animal does. theory to interpret any specific informa- Whether animals are conscious or not, tion or data set. This might at first seem we may never know for sure, but, an to make the interpretation of welfare data absence of definitive proof of animal con- simpler; when an animal appears to be in sciousness or suffering, cannot be viewed as pain, or appears to be fearful, the most a proof of absence of animal consciousness parsimonious explanation is to assume or suffering. Clearly, for zoo elephants (as that the animal is in pain or is fearful. with any other animal for that matter), we However, the principle of parsimony lead may never be able to definitively prove an to the development of Cartesian theory in individual is suffering as a result of spe- the 17th century which would lead to an cific variables associated with captivity for entirely different interpretation of the the reasons outlined and the small sam- same scenario. Rene Descartes argued ples sizes available. However, despite the that animals simply responded to external limitations of each individual measure, stimuli in a mechanistic manner and felt when we consistently record a number of that to involve consciousness was not the diverse indicators of impoverished wel- most parsimonious way in which to inter- fare, I believe it is in fact the parsimonious pret animal behaviour. Remember, the view to give the animal the benefit of the welfare of an animal is defined by what an doubt and assume that welfare is likely to animal feels, not what it does, and so con- be compromised unless there is sufficient sciousness is in fact a prerequisite of suf- evidence to the contrary. Furthermore, fering, in other words, the animal has to even in the absence of data, I do not think be aware of its impoverished state for its it is unreasonable to adopt a precau- welfare to be truly compromised. Car- tionary approach and attempt to provide tesian theory, in suggesting that animals for certain key behaviours in captivity are not conscious questions their ability to which one can reasonably argue are likely suffer, in other words they may do, but to be important to the animal as has been not feel. It has been argued that because previously described. humans and animals are related, have Given the nature of zoo elephants, the brains, nerves, neurotransmitters and limitations of experimental and physio- generally the prerequisites for pain detec- logical measures in terms of both imple- tion, and tend to behave in the same way mentation and interpretation, we are in reaction to what we could consider to currently heavily reliant upon behavioural be painful or stressful stimuli, that they indicators of welfare and establishing and most also feel pain. However, Harrison assessing the welfare correlates of the (1991) argues the avoidance of aversive animals’ environment, that is the say the stimuli and reactions suggestive of aver- extent to which their captive environment sion can be programmed in robots and comes close to providing the elephant seen in amoeba, neither of which have a with what we might reasonably assume strong case for the possession of conscious they ‘need’ for adequate welfare, and to awareness. Furthermore, although such some degree looking at the physical man- behaviours may well be adaptive, pain ifestations of impoverished welfare in the itself need not be. Carruthers (1989, 1992) carcasses of dead elephants. 70 ELEPHANTS AND RHINOCEROS

WHY DO ELEPHANTS POSE A WELFARE Social animals are typically more intel- CHALLENGE FOR ZOOS? ligent than non-social animals; primate Captive animal welfare is not by definition species with larger social networks tend to inevitably impoverished in comparison to have a relatively larger neocortex for that of wild animals, although there are example (Kudo & Dunbar, 2001). those who would disagree with this (see Furthermore, if we consider species Wuchet & Norton, 1995). Animals in the typically considered as intelligent (e.g. wild typically suffer predation, disease, chimpanzees, dogs, pigs, dolphins or par- parasitism, and starvation at levels far rots) intelligent solitary species, such as higher than those seen in the captivity. In the Orang-utan Pongo pygmaeus, are a southern India for example, 70% of bull rarity and probably more social or elephants will be killed at the hands of recently solitary in evolutionary terms man (Sukamar, 1992). By eliminating than one might first imagine. To function these anthropogenic and a plethora of effectively in a society, animals need to ‘natural’ stressors whilst simultaneously have a high level of understanding of con- providing captive animals the opportunity specifics (empathy), this in turn requires a to express their species typical behavioural high level of intelligence and self aware- needs, it is, in my opinion possible that we ness (consciousness) which in itself is often can actually improve captive welfare over cited as a prerequisite for suffering. Anec- and above wild conspecifics for many dotally we ‘know’ elephants are intelli- species. However, it is not acceptable to gent, they plan, they solve problems, they view gains in health care, food security or can learn a bewildering array of trained the elimination of predation in captivity behaviours and appear to understand as adequate compensation for a reduction more of our language than we do theirs! in stimulation, behavioural opportunities, The intelligence of elephants may make etc, because illness, predation or starva- them more capable of suffering, but their tion are unlikely to be chronic episodes in social complexities may make them more the wild, whereas a general maladapted- likely to suffer in zoos. In general terms, ness of the individual to captivity are the basic social unit for both African ele- likely to present chronic welfare chal- phants Loxodonta africana and Asian ele- lenges. Ensuring the benefits of captivity phants Elephas maximus is the matriarch; can be maximized whilst providing bio- a group of related cows and young led by logically appropriate environments is a more experienced mature cow. These possibly a greater challenge for elephants herds vary in number from between six to than for most species, and I will try and 40 elephants, but these family groups may explain why I believe this to be the case. also come together in extended family units or clans of up to 100 or in aggre- Elephant society and intelligence Elephants gations of up to 1000 (Nowak, 1991). are highly social animals and this presents However, nine to 11 is the norm in zoos with two problems. Firstly, the co- African elephants (Estes, 1992) and herd evolution of elephant intelligence (that is sizes recorded for crop-raiding Asian ele- to say their capacity to acquire and apply phants were reported to be around eight knowledge towards a specific goal), and (Sukumar, 1992). This organizational their brain to cope with a complex social structure presents zoos with a number of life is likely to have made them more vul- problems. Firstly, large facilities are nerable to impoverished welfare in cap- required to house the animals required to tivity. Secondly, there are considerable attempt to replicate even the smaller logistical problems of maintaining captive family units within the confines of a zoo. elephants in biologically appropriate Secondly, these units should ideally be social groups. formed of related animals rather than dis- REVIEW: ELEPHANTS CONCEPTS IN CARE AND WELFARE IN CAPTIVITY 71 parate individuals brought together at the one of the most sustainable forms of zoo. Lastly, elephants are capable of rec- enrichment available to animals (Veasey, ognizing the calls of large numbers of con- 2005; Veasey & Hammer, in press) and specifics (McComb et al., 2000) over potentially one of the most rewarding. As considerable distances (McComb et al., a result, for this and many other reasons, 2003), something for which elephants are the management of elephant societies in superbly adapted. It seems unlikely that captivity must be viewed as a cornerstone such a ‘biological expectancy’ could be of the effective management of these replicated in any meaningful way in cap- highly social species. tivity. The extent to which this impacts Whilst significant emphasis is placed upon elephant welfare would appear to be upon the matriarchal herd, largely particularly difficult to assess, but does because of the sex bias currently in zoos, not mean that it will be without we must be mindful that the ratio of bulls consequences. in captivity will grow as the number of Many of the problems zoos face in ele- successful births increases (see also Wiese phant management may be linked to the & Willis, this volume). The subsequent failure of managing elephants in appro- management of a growing bull population priate social groups. Tension and aggres- will present zoos with a far greater chal- sion between elephants will almost lenge than is presently being experienced certainly be reduced in related groups that in the management of cow herds. Bulls are have grown up together. There is a gen- typically considered as solitary, but in eral consensus, though as yet this still reality this is a convenient over-simplifi- remains unproven, that the problems cation. In the Asian elephant for example, experienced during parturition and in the at least 40% of herds had one adult male early years of life in captive elephants will within it which may have spent up to 30% be reduced if primiparous cows are able of their time there (Nowak, 1991). Bulls to witness parturition in related cows and typically grow up within a matriarchal are able to calve in the presence of experi- herd until such a time that they are either enced, related mothers. These cows may driven out by the females or depart vol- assist in the calving process (Schneck, untarily around the time of puberty. 1997) and subsequent parental care. Young bulls will often remain close by Recent estimates of captive calf mortality before joining looser groups of males in the first 5 years have been reported to (Schneck, 1997). Males within a region be as high as 47% in some populations may develop a hierarchy of sorts which is with stillbirths reported as high as 15·3% reliant upon regular though potentially (Clubb & Mason, 2003). It has been sug- infrequent contact. At around the age of gested by some that elephants and 25 years when bulls reach full sexual humans are comparatively unique in maturity, their behaviour is highly having a significant post-reproductive dependant upon their sexual state. During phase in their life, which has been inter- periods of musth, circulating levels of tes- preted as an indication of just how crucial tosterone may increase by over 100-fold a role, leadership, learning and experience (Jainudeen et al., 1972), and as a result play in elephant society (Estes, 1992). bulls become more aggressive, more wide- Growing up within a more ‘natural’ group ranging, more likely to be found associ- structure will also be important for the ating with oestrous females and generally appropriate socialization of elephants, spend less time in bachelor groups. Given critical to them learning the skills required the volatile nature of bulls, the fact they to function effectively within a herd, and typically mature earlier in captivity than to go onto to successfully reproduce. in the wild and their inherent social com- Moreover, social interaction, is perhaps plexities, managing large numbers of bulls 72 ELEPHANTS AND RHINOCEROS in captivity to a high standard will be an whether rumination is rewarding or not, immense challenge zoos need to start elephants could have a significant propor- planning for now, and which I will return tion of their time budget unoccupied in to later in this paper. captivity compared to ruminating herbi- vores feeding for comparable amounts of Ecology Elephants survive across a mas- time. Non-ruminants, such as elephants, sive range of habitats from deserts, grass- though less efficient digesters compensate land, swampland, seasonal forests, by processing larger quantities of food at tropical forest through to montane forests a higher rate (Sukumar, 1992; see also and upland moorland. The African ele- Hatt & Clauss, this volume). In the wild, phant can survive in any African habitat elephants spend 60–80% of their time for- that provides sufficient water (Kingdon, aging (Clubb & Mason, 2003), whereas in 1979), and will experience seasonal varia- captivity diet ‘quality’ in the nutritional tions that can dramatically alter their sur- sense is likely to be more concentrated roundings and subsequently their lifestyle. and as a result, consumed over a far To deal with seasonal, geographical and shorter time frame, more akin to that of even social variations, elephants have a ruminant. This may result in a time evolved to be adaptive, flexible and vacuum for elephants, whereby large por- opportunistic and to possess a compara- tions of the captive elephant’s day are left tively diverse and complex behavioural unfilled with diet acquisition and proc- repertoire when compared to most other essing, which can have profound conse- ungulates. As a result, elephants have the quences on their welfare. neurological tools and innate behavioural As far as I am aware, there have been capacity, or what amounts to an ‘evolu- no thorough investigations into the long- tionary expectancy’ to be presented with term effects of climate and photoperiod a potentially changeable and diverse set of upon the welfare of captive elephants but environmental parameters. When the it is likely that these factors will have an environment does not match that ‘evolu- impact either directly or indirectly. tionary expectancy’, suffering maybe Although both African and Asian ele- more likely, exacerbated by the now sur- phants can experience low temperatures in plus neural capacity and potentially ‘frus- certain parts of their range at certain times trated’ behaviours. of the year, they are unlikely to experience The digestive strategy of the elephant conditions equivalent to those found in may also precipitate welfare problems in many temperate zoos in winter for captivity. Unlike cattle, antelope, deer and extended periods of time in the wild. In giraffes, etc, elephants do not ruminate, humans there is evidence linking such that is to say, they do not regurgitate and temperate climates to an increased inci- re-masticate partially digested food. dence of rheumatoid arthritis (Hameed & Because rumination can be considered as Gibson, 1997), the same may or may not a vital component of ruminant feeding be true for elephants (see Clubb & Mason, behaviour, it is not unreasonable to 2003), but nonetheless, arthritis is believed assume that it is likely to be rewarding to by Fowler (2001) to be one of the main perform, but even if this is not the case, it reasons for euthanasing elephants in cap- is effective in occupying the time of cap- tivity. If it does not have a direct impact, tive ruminants. Captive Giraffe Giraffa climate might still compromise the welfare camelopardalis, for example, ruminate for of elephants indirectly by forcing them to as much as 40% of observation periods be kept inside for prolonged periods of (Veasey et al., 1996b), and Eland Tauro- time. This may result in a reduction in tragus oryx feed and ruminate in equal activity levels and behavioural oppor- amounts (Estes, 1992). As a result, tunities, combined with an increased level REVIEW: ELEPHANTS CONCEPTS IN CARE AND WELFARE IN CAPTIVITY 73 of exposure to unnatural and potentially in locating them. Moreover age classifi- more challenging substrates and cation in adult elephant carcasses is suf- surroundings. ficiently difficult that mortality studies include classes as broad as ten and over Health care Our understanding of ele- (Douglas-Hamilton, 1972; cf Clubb & phant health care and its management is Mason, 2003). Whilst longevity in cap- not yet at the level it is for domesticated tivity (and even the wild owing to a high species or their relatives. As a result, the proportion of anthropogenic mortality) is rate of undetected or unsuccessfully man- not acceptable, it is in fact potentially aged disease events is potentially higher comparable. However, typically, most zoo than it might be for a zoo bovid for animals live far longer than their wild example. Over 60% of adult elephant counterparts and the same should be deaths in captivity can be attributed to attainable for elephants, and is possible as disease (Clubb & Mason, 2003) which is can be demonstrated by the increased lon- not entirely surprising, or indeed worrying gevity seen in timber-camp elephants com- because non-accidental death is typically pared with those in zoos (Clubb & precipitated by, or coincidental with dis- Mason, 2003; Sukumar, this volume). ease in any circumstance. However, when one considers the age of onset of these Management in zoos The manner in fatal diseases, there would appear to be which we manage elephants in captivity some cause for concern. If we accept the will have a dramatic effect upon their life- data of Clubb & Mason (2003), the life style. We know elephants live complex expectancy for captive Asian elephants is social lives in the wild (and I would 21 years and 18 years for African ele- include bulls in that statement), and we phants when death at less than 1 year old know that they spend a significant pro- is excluded, this compared to a life expect- portion of their time foraging and feeding, ancy of up to 70 years in the wild (but see both areas of high survival value and Wiese & Willis, 2004). However, care therefore likely to be of high welfare must be taken when comparing a significance. In captive scenarios, where maximum longevity with a mean life management results in the restriction of expectancy. For example, whilst elephants feeding, foraging and social opportunities can live to 70 years of age in the wild, in welfare problems are most likely to occur. recent years wild populations have been in Clearly the training and handling of ele- decline, and so the average elephant is phants in captivity can have profound dying prior to reproduction, which with welfare implications, both positive and sexual maturity being reached at negative. Training exists across a con- 14–22 years old (Sukamar, 1992; Nowak, tinuum from comparatively intense hands 1997) suggests the average elephant is on or free contact training where the unlikely to survive much beyond its teens. trainer works ‘unprotected’ with the ele- Data for wild African elephants suggests phant, typically with the use of an ankus an average life expectancy (excluding or elephant hook, through to protected animals which died at under 1 year old) of contact where a barrier is present between 21·8 years (Laws et al., 1975), comparable trainer and elephant and zero contact with that seen in zoos. If we analyse where no training is attempted. Where Sukamar’s (1992) data for wild Asian behaviours are trained, they typically are bulls, we see average age at death is under reinforced via the use of the ankus and or 23 years. However, these may well be the provision of positive reinforcement; overestimated because early deaths will be generally food rewards or positive feed- underestimated owing to the more rapid back from the keeper. Potential positive deterioration of carcasses and difficulties aspects of training include the ability to 74 ELEPHANTS AND RHINOCEROS impose exercise regimes on animals that amongst zoo animals and appears to orig- might otherwise be inactive, the mental inate from traditional management tech- stimulation potentially offered by niques used to manage working elephants training, the opportunity for elephants to in Asia and in circuses. As yet, there experience more diverse surroundings by appears to be little common ground moving them outside of their enclosures, between the advocates for and against the management of chronic health-care free-contact training, however, both sides issues without the need for chemical must surely agree that the benefits to the immobilization and the opportunity to elephant of training, through which ever develop positive relationships with technique, must outweigh the potential keeping staff, etc. costs to the elephant, and if not, there has The potential negative welfare aspects to be an aspiration to achieve this point. of the reliance upon training are however, However, what is not acceptable, is to also numerous. Animals denied choice excuse deficiencies in facilities or captive and control over their surroundings, are elephant lifestyles by provisioning the ele- likely to suffer a reduction in welfare and phants with gains delivered through thus although the opportunity to explore training. Thus chronic confinement to outside of the elephant’s enclosure can be inadequate facilities should not be justi- viewed as a welfare asset, the fact it has fied by occasional walks outside of those to be at the behest of the keeping staff and confines. very much on their terms, will diminish Circulatory problems appear to be the the welfare benefit. Training is a skilled most significant cause of death in zoo ele- and time-consuming process, which phants (Clubb & Mason, 2003) which in although can fill voids potentially left by humans at least, can be precipitated by the lack of behavioural opportunities in chronic stress and obesity and could thus captivity, can also result in the albeit tem- potentially be hastened by inadequate porary, but nonetheless frequent involun- management strategies and facilities. The tary separation of close-knit social units, second biggest cause of morbidity, but with potentially significant welfare conse- perhaps the biggest single health problem quences (Clubb & Mason, 2003). The in Asian elephants are foot problems apparent reliance on ‘punishment’ as a (Schmidt, 1986; Fowler, 2001) with as training mechanism, is perhaps the most many as half of all captive elephants suf- emotive dimension of elephant training. fering from foot problems at any one time Positive reinforcement, that is to say, the (Mikota et al., 1994). Factors which are reinforcement of desired behaviours by likely to predispose elephants to foot the provisioning of a reward is prob- problems are a lack of exercise potentially lematic for bulk vegetarians such as the combined with excess body mass, elephant which can consume up to 300 kg improper, unhygienic or excessively moist per day, because each food reward will substrates, climate and the performance of always be a minute fraction of their daily stereotypic behaviours (Clubb & Mason, intake and as a result, of limited signifi- 2003). So many of these factors are intrin- cance. Given the nature of elephants and sically linked, and precipitated by both the potential limitations of positive management practices and environmental reinforcement, keeper safety in free-con- variables that at least for the Asian ele- tact systems typically relies at least in part phant, the occurrence of foot problems on a degree of negative reinforcement might even be viewed as a crude welfare whereby undesirable behaviours are pun- barometer. Inactivity prevents appro- ished generally mediated through the use priate wearing down of the footpad and of the ankus. Such an approach to toe nails, and predisposes the animal to management is comparatively unique obesity that puts additional strain on REVIEW: ELEPHANTS CONCEPTS IN CARE AND WELFARE IN CAPTIVITY 75 inadequately exercised joints and tendons. welfare is consistently an important con- These problems may be exacerbated by sideration in the mindset of elephant poor substrate choice or maintenance and management teams, but I suspect it is not the performance of stereotypic behaviours always ‘the’ most important factor, or if that may cause uneven and excess wear. it is, it is often the most important factor Again, an understanding of species within the constraints of institutional con- biology is vital. The differences in occur- siderations or limitations and often based rences and nature of foot problems in cap- on how it has always been done. It is tive African and Asian elephants may be unacceptable for institutions to try and do attributable to their ecology rather than the best they can in perpetuity if this infra- their management. African elephants structure falls below what is required to range widely over rough terrain and as ensure adequate welfare standards are such would appear to have more robust maintained. Deciding what is required pads prone to overgrowth in zoos, and what is adequate, is of course a major whereas Asian elephants inhabit arguably challenge in itself, however, in the absence less abrasive environments in the wild and of data, institutions or regional associa- regularly forage by raking and kicking at tions need to establish sensible, but in grasses and herbage and so have evolved reality, what will be challenging minimum nails which grow more rapidly and thus standards to which institutions must reach require trimming in zoos (Clubb & within a reasonable time frame, or decide Mason, 2003). Management should of not to keep elephants if they cannot attain course reflect these differences. The recent those standards. In the UK, the BIAZA construction of facilities with sand sub- guidelines have taken an important first strates inside appear to show considerable step towards that end (Stevenson & promise in terms of improving foot con- Walter, 2006), and a number of zoos have dition in captive elephants. If designed responded by taking the brave decision of correctly these are free draining, inter- ‘going out’ of elephants, or perhaps the active surfaces which spread the load even braver decision of striving to meet or across the entire foot surface and facilitate surpass those standards. However, setting lying down in a way concrete substrates meaningful evidence-based standards is a do not. difficult task because elephant welfare is so evidently multifactorial and highly THE FUTURE complex. Thus minimum indoor facility I suspect this document will have raised sizes need to reflect climate and time more questions than it has answered animals will be kept indoors, and regarding elephant welfare in captivity although size is an easy variable to and its management. However, although measure, enclosure complexity and design clearly the management of captive ele- are also critical. So, although we have to phant welfare is a significant challenge, I accept that deciding what elephants need do not believe it to be a theoretically or where we set the standards will be chal- insurmountable one given the will, the lenging or inevitably controversial, I financial commitment and an open mind. would offer the following suggestions in Perhaps the first step forward (for those anticipation of further advances in our who have not already undertaken this) is understanding of captive elephant to completely re-evaluate institutional ele- management, and thus more stringent evi- phant management strategies putting the dence-based guidelines. welfare of the elephants at the absolute Everyone involved in the management core whilst avoiding being unnecessarily of elephants has to be open-minded to restricted in our deliberations by what we novel approaches to management. Too already do and why we do it. Elephant many of our current management 76 ELEPHANTS AND RHINOCEROS strategies are relics of circus-management compatible herds covering a number of practices, particularly with regards to the generations. In the long term, zoos will management of Asian elephant and their need to ‘grow’ these herds through feet. We train elephants for many reasons, breeding but for the immediate future but in reality, the only acceptable justifi- these will probably need to be established cation for free-contact management in by co-operatively experimenting with particular, as a result of its inherent combinations of cows already in zoos to human health and safety risks and poten- ensure, if at all possible, compatible herds tial elephant welfare costs, has to be to can be developed. Too many zoos appear optimize the welfare of the elephants to accept the fate of lone elephants or within an institution. Thus the potential pairs of elephants within their ‘herd’ that welfare costs of training can only be jus- are not compatible with the remaining tified, in my opinion, if there is a clear net animals. Such an approach would not be welfare benefit to that training. Human possible and certainly not desirable in health and safety should not be a justifi- many (if any) other social species in zoos, cation for free-contact management so why elephants? Zoos need to consider because this should be managed through the herd as the focus, rather than facility design as it is with all other dan- becoming overly fixated or too attached to gerous animals within zoos. All other jus- particular animals to the detriment of tifications which relate to the elephant judicious regional management. Likewise, rather than humans worthy of consider- reproductive planning on an institutional ation can surely be overcome by research basis must coincide with strong, long-term leading to improvements in husbandry regional collection planning and studbook and design. Given the health problems in management to support the aspiration to captive elephants and most notably foot ‘grow’ and manage biologically appro- problems in Asian elephants, free-contact priate herds. Thus moving single young management strategies can of course be cows to other institutions should not extremely useful in the treatment of these occur (unless incompatibilities develop, and a multitude of other problems. How- which should not be the case within a ever, it has to be the aspiration, whether related herd), but rather trios or more of it is achievable or not, to work towards compatible, related elephants should be reaching a point where free-contact management and training as we now moved on to form the nucleus of new know it is effectively obsolete because the herds. Once zoos reach carrying capacity, environment we are capable of providing assuming there is not a demand for cap- our elephants is such that regular inter- tive-bred elephants in range states (and vention is not required. Likewise, the envi- culling is still considered unacceptable for ronments we provide elephants should be elephants), reproduction will probably sufficiently socially and physically com- need to be managed in such a way that plex and enriching that we do not need to each herd is self-sustaining with birth walk them around the zoo or further a rates being equivalent to mortality rates field (always on our terms) to ensure their whilst maintaining a stable age pyramid. welfare is optimized. In order to work Thus, matriarchal herds would be com- towards this point we really have to paratively stable with the movement of address the inadequacies of the elephant’s bulls between zoos maintaining the environment in captivity from a social and genetic integrity of the population. The physical perspective. low rate of reproduction required will be To achieve this elephants will have to a cause of concern in relation to repro- be maintained in biologically appropriate ductive senescence, social enrichment and units. For females this will mean related, learning, etc, but in the absence of culling, REVIEW: ELEPHANTS CONCEPTS IN CARE AND WELFARE IN CAPTIVITY 77 and an outlet for captive bred elephants, Such an approach, is more natural in the I see little alternative. sense of bulls visiting stable cow-based Clearly, for the foreseeable future, herds, and likely to be more successful reproduction in captivity is likely to yield than moving individual cows from a herd at least as many bull calves as cows, which situation to be mated by a bull elsewhere. is more than zoos need or can currently Thus any collection which wants to breed handle. As a result, zoos either need to elephants should plan for ‘difficult’, develop an ethically acceptable manner in ‘hands-off’ bulls rather than relying on which the proportion of bull calves born cows being moved on for breeding or on can be reduced or culled, or develop a artificial insemination. I also think it long-term strategy for the management of appropriate, that zoos which attempt to a large and growing population of bulls hold bachelor herds, and in doing so, help within zoos. It is conceivable, though cur- to solve a potentially very difficult and rently unlikely that zoos could play a role growing issue for zoos, be collectively in repopulating bulls in Asia where they compensated by those institutions have historically been reduced by sex- focusing primarily on cow herds. Initial biased poaching for tuskers resulting in a trials in Spain with young Asian bulls, heavily skewed sex ratio. However, for a appear promising but only time will tell multitude of reasons, this is unlikely to whether or not these will work in the occur in the short to medium term and longer term as the bulls mature. would require well-adjusted, socialized The management of elephant diets in bulls that had grown up in appropriate captivity is also ripe for improvement, and social scenarios, not to mention consider- not just from a nutritional perspective. In able levels of funding from zoos. order to manage elephant welfare in cap- At this time, it is difficult to hypothesize tivity, zoos should strive to replicate ele- what the answer might be for bull ele- phant feeding ecology in the wild. To do phants and their management in captivity, this zoos need to dissipate feeds both spa- but I suspect facilities with large, complex tially and temporally from ‘events’ to a spaces in warmer climates may provide continuous, omnipresent opportunities the best chance to experiment with bach- and should include feeds outside of zoo elor herds. Ideally the bulls would be pro- working and opening hours. Thus ele- vided with the space and environmental phant feeding should take up the majority complexity (topography, vegetation, of the animals’ time in captivity without visual barriers, etc, and physical separa- predisposing them to obesity. Thus ‘low- tion when required) to avoid each other quality’ bulk feeds spread through out the when needed, but also the opportunity to day should be provided, preferably where choose contact when desired. Ideally, they the elephant is required to manipulate, should be in a region less reliant upon process or work for the food. This has indoor facilities because these animals will additional benefits other than keeping the almost inevitably have to be managed in elephant active. By reducing the signifi- a comparatively hands off manner owing cance of individual feeds, aggression com- to the space required and the fact that monly reported in captive herds at feeding they are bulls. These herds could not only time may also be dissipated, and could then attempt to address the surplus bull facilitate a more cohesive herd structure issue, but also provide zoos with the within captivity. Increasing the time occu- genetic resources they can utilize when pied by this inherently rewarding behav- needed for breeding. Thus bulls from iour, also reduces the opportunity for these hypothetical herds could be selected elephants to develop other ‘vices’ such as to visit cow herds on a breeding loan or destroying infrastructure and stereo- to remain on a more permanent basis. typing. Access to a natural grazing sub- 78 ELEPHANTS AND RHINOCEROS strate is the most obvious solution to this, the way forward seems (to me at least) but something that can only be realisti- surprisingly clear and entirely obvious. In cally achieved for the ultimately desirable my opinion, if zoos can provide elephants larger herds in extensive areas. It would with environments that are sufficiently certainly be advantageous, if not neces- large and complex to be capable of sus- sarily attainable for all elephant holding taining the grazing pressure of func- facilities to provide their herds (which tioning, biologically appropriate social should be of a biologically relevant size) units which feed for the majority of any with sustainable areas for grazing because given day, for the majority of the year, the space provided will also allow for without predisposing the animals to any behavioural opportunities over and above health defects then I believe we could feel that relating to feeding. far more confident about the welfare of In order to ensure elephants are active elephants in our care. 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