124 ZOO CHALLENGES: PAST, PRESEh-T A N D F L T U R E

M. (Eds). Washington, DC: Smithsonian Institution Press. SHEPHERDSON, D. & CARLSTEAD, K. (2000): When did you last forget to feed your tiger? Raising the bar on environmental enrichment in AZA zoos and aquaria. AZA Annual Conference Proceedings 2000: 23 1-235. SHEPHERDSON, D. J., CARLSTEAD, K., MELLEN, J. D. & SEIDENSTICKER, J. (1993): The influence of food presentation on the behavior of small cats in con- fined environments. Zoo Biology 12 203-216. SHEPHERDSON, D. J., MELLEN, J. D. & HUTCHINS, M. (Eds) ( 1998): Second nature: environmental enrich- ment ,for cuptive animals. Washington, DC: Smith- sonian Institution Press. STARK, B. (Ed.) (1999): Enrichment notebook (2nd edn). Topeka, KS: American Association of Zoo Keepers. SWAISCOOD, R. R., WHITE, A. M., Znou, X., ZHANG, H., ZHANG, G., WEI, R., HARE, V. J., TEPPER, E. M. & LINDBURG, D. G. (2001): A quantitative assess- ment of the efficacy of an environmental enrichment

programme for giant pandas. Animal Behnviotrr 61: 441451. WEMELSFELDER, F. (1993): The concept of boredom and its relationship to stereotyped behavior. In Ster- eotypic behaviour: fundamentals and applications to animal welfare: 65-96. Lawrence, A. B. & Rushen, J. (Eds). Wallingford, Oxon: CAB International. WEMELSFELDER, F., HASKELL, M., MENDL, M. T., CALVERT, S. & LAWRENCE, A. B. (2000): Diversity of behaviour during novel object tests is reduced in pigs housed in substrate-impoverished conditions. Aniniul Behaviour 6 0 385-394. WIELEBNOWSKI, N. C. (1999): Behavioral differences as predictors of breeding status in captive cheetahs. Zoo Biology 18: 335-349. WIESE, R. J., WILLIS, K. & HL~TCHINS, M. (1994): Is genetic and demographic management conservation? Zoo Biology 13 291-299. YERKES, R. M. (1925): AlmoJt hunian. Neur York: The Century Company.

Manuscript submitted 18 January 2001; accepted 5 March 2001

Int. Zoo Yb. (2003) 3 8 124130 0 The Zoological Society of London

Welfare, husbandry and veterinary care of wild animals in captivity: changes in attitudes, progress in knowledge and techniques J. K. KIRKWOOD The Universities Federation for Animal Welfare, The Old School, Brewhouse Hill, Wheathumpstead, Hertfordshire AL4 8AN, United Kingdom

Since the first zoos were founded, attitudes to keeping wild animals in captivity have changed con- siderably. A much firmer conviction that animals have the capacity for consciousness and thus suf- fering, has been one factor in the growth in concern for welfare in recent decades. The pursuit of conser- vation goals and higher welfare standards has driven remarkable advances in the husbandry, veterinary science and care of wild animals.

Key-~vovc/s; health, husbandry, legislation, prefer- ences, rights, veterinary care, welfare

The last decades of the second millennium may well be remembered long into the

future as the time when the human popu- lation first woke up to the scale of its impact on other animal species, and to the practical and ethical implications of this. With the human population passing the 6 billion mark in the final months of 1999, major conflicts between human and animal interests have become widely apparent (see also Conway, this volume). Concerns about loss of animal popu- lations and species have given rise to the conservation movement. At the same time disquiet about harm caused to the quality

REVIEW WELFARE, HUSBANDRY A N D VETERINARY CARE 125

of life of the enormous numbers of animals utilized in support of, or over- whelmed by, the vast human population have led to growing concern for animal welfare. Zoos have found themselves in an interesting position at this time. Increas- ingly, the maintenance of captive popu- lations has become accepted as -a component of the strategy for the conser- vation of some species while, simul- taneously, a great deal of public concern has been focused on the welfare of captive wild animals. Attitudes to animal welfare have changed markedly in many parts of the world in recent decades. The back- ground to this change and the conse- quences of it for developments in wild-animal care, in zoos and elsewhere, are outlined in this article.

ATTITUDES TO ANIMAL WELFARE Concern for animal welfare is largely about concern for the feelings of animals (Dawkins, 1990; Fraser & Duncan, 1998). This concern is based on the belief that animals, or at least some of them, have the capacity for conscious awareness of pleasant and/or unpleasant feelings Gust as humans do) and that they can suffer if their welfare is poor and/or have pleasant feelings when their welfare is good. Health is an aspect of welfare but welfare is not synonymous with health. Health is a con- cept that applies equally to plants but wel- fare is not. There can be many good reasons to protect and tend living things, including non-conscious organisms, care- fully and conscientiously (e.g. conserva- tion) but unless it is believed that they have, or may have, conscious feelings, concern for welfare is not one of them.

Historically, at least in western culture, doubts and uncertainties about conscious- ness in non-human animals, or that the moral consequences of this were an important matter for concern, have been voiced frequently. Various influential philosophers, theologians and scientists have at times, in raising these doubts, fos- tered disregard for the importance of the

welfare of animals (see reviews by: Hume, 1962; Rollin, 1989; Griffin, 1992). It may be an over-simplificai ion to ascribe the recent and widespread change in attitude to animal welfare to one factor alone but the much firmer conviction that animals have the capacity for consciousness and thus suffering, which arose through the development of biological science, may well have been a key component. In showing that humans had common ancestry with other animals, Darwin did much to open minds to the possibility that consciousness had evolved long before humans. Since then, iiicreasingly compel- ling evidence for the latter has emerged from a variety of branches of study (e.g. Dawkins, 1993; Churchland, 1996; Baars, 1997; Weiskrantz, 199‘7). It was something of a landmark in the progress of the legal underpinning of the humadanimal relationship when, a.t the Amsterdam Summit meeting in 1997, the European Heads of State agreed to make provision in the Treaty of Rome (the Treaty which established the European Community in 1957) ‘to ensure improved protection and respect for the welfare of animals as sen- tient beings’.

At time of writing some animal housing and husbandry systems in use on farms, in zoos and for companion animals, have their origins in a time when attitudes to animals were different to those which are prevalent today. Until the comparatively late stages of the 20th century the scien- tific and philosophical ambience was such that the focus of animal husbandry was mainly on physical health and produc- tivity. The principal considerations in the design of zoo-animal housing used to be function, hygiene and, perhaps, architec- tural aesthetics, however, now much greater account is taken of the physical and psychological needs of the animals, at least in the better zoo:; (Shepherdson, this volume).

Similarly, until recent decades, it seems that for the most part little effort was put into the study of methods of care and hus-

126

bandry of animals in zoos. When deaths occurred, more effort was often centred on acquiring replacement animals than on investigating the causes of death and developing improved management and veterinary technology. This may sound overly harsh, especially as I am sure that zoo managers and keepers have always tended to be fond of their animals and to have done what they could to take good care of them. However, attitudes as to what constitutes acceptable and good standards of animal care have certainly changed. This is not something peculiar to zoos. Systems of animal keeping on farms, in laboratories and as pets in the home have been subject to corresponding scru- tiny, re-evaluation and redevelopment in the light of growing knowledge of animal biology and the ethical implications of the deeper understanding of welfare needs that this has brought about (see also Ste- vens & McAlister, this volume).

DEVELOPMENTS IN HUSBANDRY A N D VETERINARY CARE Stimulated by concerns for both species conservation and animal welfare, devel- opments in the technology of keeping wild animals in captivity during the last half century have been truly remarkable. Advances in, for example, nutrition, chemical restraint and anaesthesia, knowl- edge of infectious and non-infectious diseases and their treatment and preven- tion have been profound. There has been a marked growth in research into aspects of zoo-animal biology, husbandry and medicine, and many zoos have established research departments or, at least, links with local universities. Many advances in the zoo veterinary field have come about through developments from new tech- nology in human and domestic-animal medicine. For example, almost all the val- uable range of drugs now used for the chemical restraint and anaesthesia of zoo animals, and the treatment and prevention of infectious diseases, were initially developed for human or domestic-animal

use. The existence of zoo-based research and clinical groups associated with some of the larger zoos has facilitated this transfer and adaptation of technology. However, there has been a two-way flow: research groups that were established ini- tially to address zoo problems have often been able to find resources to enable the expertise developed ‘in house’ to be applied to field conservation or other val- uable scientific collaborations.

It is only because we know what we do now that we can appreciate how much less was known 50 years ago and how serious the gaps in knowledge and technology were in the past. Advances in the science of ecology have provided a much better appreciation of the level of precision to which species are adapted to their natural environments; particularly to coping with potential harms and exploiting potential benefits associated with the climate, food resources, predators, parasites and infec- tions, and other features of the environ- ment. This information, together with greater knowledge and experience of the potential difficulties of keeping wild animals in captivity, has engendered a more cautious approach to wildlife inter- ventions which involve bringing animals into captivity, even for short periods. For example, awareness of the complexities and potential difficulties of nutrition and of the potentially disastrous consequences of the spread of novel infectious agents into new host species or new ecosystems (Daszak ef al., 2000) has made the appar- ently casual and constraint-free expedi- tions for the collection of wild animals for zoos described in former days seem parti- cularly naive. The recognition of potential threats to animal health, welfare and con- servation has resulted in a considerable body of legislation at both national and international level which regulates the shipment of wild animals (Brooman & Legge, 1997; Kirkwood, 2000a). However. animal-health legislation in this field has been developed largely for the protection of production animals and humans. The

REVIEW WELFARE. HUSBANDRY AND VETERINARY CARE 127

legislation tends to be somewhat blind to the possibility of accidental introduction of diseases which may affect captive or free-living wildlife and may not provide protection against this. Statutory quar- antine, screening and prophylactic meas- ures may be inadequate and should be augmented where necessary.

From the perspective we have now, maintaining wild animals in captivity is not as simple and straightforward as was believed 50 years ago. Where species are maintained in zoos as part of conservation programmes, the aim is to minimize genetic change from that of the wild founder populations. In addition to care- fully managed breeding, this requires high standards of husbandry because, if the captive environment is not designed to suit the species, natural selection will tend to ‘engineer’ the population to fit its environment. The resulting captive- adapted strains may then be less suited to the natural environment should there be a need for reintroduction (see also Stanley Price & Soorae, this volume).

Although there is greater awareness of the potential difficulties there is also much more information available as to how many of these can be overcome. There have been great advances in diagnosis, in understanding the epidemiology and in methods of treatment and prevention of many diseases. It is not possible to pro- vide here even a cursory review of the now large and rapidly expanding field of hus- bandry and veterinary care of captive wild animals. However, among the valuable sources of information are the Znter- national Zoo Yearbook (see also Olney, this volume), the Journal of Zoo and Wild- life Medicine, Zoo Biology and Animal Welfare; the last three of which were launched during the last 20 years. Several highly valuable compendia on aspects of husbandry and medicine have been pub- lished in recent years (e.g. Ritchie et al., 1994; Kleiman et al., 1996; Mader, 1996; Field, 1998; Fowler & Miller, 2000). Some discoveries have had a huge impact. For

example, although there are many thriving populations of New World pri- mates in captivity now, before the dis- covery that these primates differed from their Old World relatives in being unable to utilize vitamin D, and in requiring die- tary vitamin D,, there had, not surpris- ingly, been little success in maintaining and breeding marmosets and tamarins in captivity (Hunt et al., 1967; Crissey et al., 1998; Crissey & Pribyl, 2000).

In addition to research aimed at deter- mining the requirements for physical health, there has also been growing con- cern to meet behavioural (psychological) needs. It has become clear that some animals have a strong motivation or need to perform certain behaviours even when these are functionally redundant in a cap- tive environment. Stereotypic behaviours may be a means of alleviating or coping with unpleasant mental states which may occur if attempts to perform natural behaviours are thwarted (Mason, 1991). Research in various fi1:lds of zoo biology has helped, or begun to help, clarify and define what the captive environments of particular species should and should not include, although much more work still remains to be carried out (Robinson, 1998).

It is not easy to know what animals need and want or whether what they want is good for them. Nor is it easy to tell, without detailed veterinary and behav- ioural studies, when the captive environ- ment is right for the welfare of an animal (Kirkwood, 1999). There has been a move, particularly in farm and laboratory animal husbandry, towards ‘asking’ the animals by using preference tests to reveal their choices about various aspects of the accommodation (Dawkins, 1990; Fraser & Matthews, 1997). For example, given the choice, do the animals prefer a small or a large space, and how hard are they prepared to work, say in terms of pressing a lever, for such preferences? Studies aimed at answering these questions can reveal which features of a captive environ-

128 ZOO CHALLENGES. PAST. PRFSENT A N D FUTCIKt

ment are important to the occupants and to what extent. Despite some limitations (Dawkins, 1990; Fraser & Matthews, 1997), this approach will probably, in the long run, contribute to the development of improved housing and management of wild animals in captivity (e.g. Hosey et al., 1999).

It seems highly likely that pleasant and unpleasant feelings evolved as carrots and sticks to help guide an animal’s behaviour in a way that maximizes its evolutionary fitness (production of viable offspring). Therefore, in general, providing an environment which meets an animal’s cog- nitive needs (that is, which provides it with what it wants) is likely to be good for its welfare and health (Duncan & Petherick, 1991). However, the match between what an animal wants and what is good for it is unlikely to be exact in an artificial environment. Feelings evoked by stimuli that were not present in the environment in which a species evolved may be inappropriate. For example, nic- otine, heroin and some other psycho- active drugs may induce pleasure in humans while severely reducing evolu- tionary fitness. Similarly, animals have not evolved detection mechanisms, let alone aversive feelings, to some harmful environmental pollutants, such as lead or polychlorinated hydrocarbons, that they may encounter in the modern world (in captivity or the wild) and so may make wrong choices about what is good to eat.

THE FUTURE On the one hand we are much more aware of the many kinds of problems that can arise when wild animals are kept in cap- tivity and which may compromise the via- bility of captive populations and/or the welfare of the animals in them. On the other hand, we are much better equipped, in terms of knowledge and technology, to deal with many of the more common and tractable of these problems. Although there has been a huge leap forward in recent decades, the care of captive wild

animals is a comparatively young branch of animal husbandry and there is still a great deal to learn. Compared with what is known about the biology and needs of humans and domestic animals, knowledge of many species maintained in zoos remains scant.

The growing human population is likely to result in increasing threats to wild animals, particularly the viability of many species and the welfare of large numbers of individuals (Sainsbury et al., 1995). Some have argued against keeping wild animals in captivity. The philosopher Tom Regan wrote of wild animals ‘the general policy recommended by the rights view is: let them be!’ (Regan, 1983). How- ever, 6 billion people cannot and will not just let wild animals be, even if they wished that they could. Humans are, whether we like it or not, in competition with many other species for food, space and other finite resources. We have not succeeded in avoiding causing harm to wild animals and are extremely unlikely to completely succeed in this in the foresee- able future, if ever. There are times when we must either intervene to try to deal with the problems we cause, or risk exac- erbating harms to welfare and conserva- tion through neglect (Kirkwood, 2000b).

Modern zoos form part of the com- munity working for species conservation through the promotion of interest and knowledge about wild animals, and run- ning or supporting direct measures. Direct conservation measures may involve various interventions, such as transloca- tions, captive breeding and reintro- duction. At times, it may be important to undertake research involving procedures, such as the collection of blood samples, to determine threats to population viability (e.g. infectious diseases). While all these activities may be directed towards species conservation, they may not all be in the best interests of the individual animals involved. Regan (1992) argued that for animals ‘The rights of the individual are not to be violated in the name of some

REVIEW WELFARE, HUSBANDRY AND VETERINARY CARE 129

collective good, whether that good be the good of the ecosystem or the good of sen- tient life (both human and non-human), and independently of whether these rights are violated ‘humanely’ or otherwise.’. However, at present, most societies allow a more flexible stance which permits that an animal’s interests may, under some cir- cumstances, be compromised (within limits) providing that the benefits out- weigh the welfare costs.

It is probable that maintaining popu- lations of wild animals in captivity will continue to be valuable for conservation and education reasons. It is important that (1) the actual and potential benefits and welfare costs, and the ‘balance’ of these, are kept under regular and careful review, and (2) steps are taken to mini- mize all welfare costs through high stan- dards of husbandry and medicine and, where necessary, through further research into the physiological and psychological needs of the animals and how these can be met.

REFERENCES BAARS, B. J. (1997): In the theater of consciousness: the workspace of the mind. Oxford: Oxford Univer- sity Press. BROOMAN, S. & LEGGE, D. (1997): Law relating to animals. London: Cavendish Publishing Limited. CHURCHLAND, P. M. (1996): The engine of reason, the seat of the soul. Cambridge, MA: MIT Press. CRISSEY, S. & PRIBYL, L. (2000): A review of nutri- tional deficiencies and toxicities in captive New World primates. International Zoo Yearbook 31:

CRISSEY, S., PRIBYL, L., PRUETT-JONES, M. & MEEHAN, T. (1998): Nutritional management of Old World primates with special consideration for vitamin D. International Zoo Yearbook 3 6 122-130. DASZAK, P., CUNNINGHAM, A. A. & HYATT, A. D. (2000): Emerging infectious diseases of wildlife- threats to biodiversity and human health. Science 287: 4 4 3 4 9 . DAWKINS, M. S. (1990): From an animal’s point of view: motivation, fitness and animal welfare. Behuv- ioural and Brain Sciences 1 3 1-61. DAWKINS, M. S. (1993): Through our eyes only? The search for animal consciousness. Oxford: W. H. Freeman & Co. DUNCAN, I. J. H. & PETHERICK, J. C. (1991): The implications of cognitive processes for animal wel- fare. Journal of Animal Science 69 5017-5022.

3 5 5-360.

FIELD, D. A. (Ed.) (1998): Caidelines for enrichment. Chester: Association of British Wild Animal Keepers. FOWLER, M. E. & MILLER, R. E. (Eds) (2000): Zoo and wild animal medicine: current therapy (4th edn). Philadelphia: W. B. Saunders Co. FRASER, D. & DUNCAN, I. J . H. (1998): ‘Pleasures’, ‘pains’ and animal welfare: towards a natural history of affect. Animal Werfare 7: 383-396. FRASER, D. & MATTHEWS, I,. R. (1997): Preference and motivation testing. In Animal welfare: 159-173. Appleby. M. C. & Hughes, 13. 0. (Eds). Wallingford: CAB International. GRIFFIN, D. R. (1992): Animal minds. Chicago: Uni- versity of Chicago Press. HOSEY, G. R., JACQUES, M & BURTON, M. (1999): Allowing captive marmosets to choose the size and position of their nest box. Animal Welfare 8: 281-285. HUME, C . (1962): Man and beast. London: Univer- sities Federation for Animal Welfare. HUNT, R. D., GARCIA, F. G. & HEYSTED, D. M. (1967): A comparison of vii.amin D, and D, in New World primates. 1. Production and regression of osteodystrophia fibrosa. Laiioratory Animal Care 17: 222-234. KIRKWOOD, J. K. (1 999): Design of accommodation for wild animals: how do we know when we have got it right? In Conservation centres for the new mil- lenium. Proceedings of tht , 5th international sym- posium on zoo design. Paignton Zoological and Botanical Gardens, 18-2.? May 1998: 51-61. Plowman, A. B. & Stevens, P. M. C . (Eds). Paignton: Whitley Wildlife Conservation Trust. KIRKWOOD, J. K. (2000a): Veterinary considerations and ethical dilemmas in vertebrate reintroduction programmes. In Bringing buck the bison. Proceedings of a symposium jointly orgarrised by Marwell Zoolog- ical Park, The Defence Evaluation and Research Agency, and The Wildlife Conservation Foundation: 1-2 October 1998, Farnborough: 30-35. Langenhorst, T. & Wakefield, S. (Eds). Colden Common: Marwell Preservation Trust. KIRKWOOD, J. K. (2000b): Ethical aspects of inter- ventions for the conservation or welfare of wildlife. In Veterinary ethics-an introduction: 121-138. Legood, G. (Ed.). London: Cassell. KLEIMAN, D. G., ALLEN, M . E., THOMPSON, K. V. & LUMPKIN, S. (Eds) (1996): Wild mammals in cap- tivity: principles and techniques. Chicago: University of Chicago Press. MADER, D. R. (Ed.) (1996): Reptile medicine andsur- gery. Philadelphia: W. B. Saunders Co. MASON, G. M. (1991): Stereotypies and suffering. Behavioural Processes 25: 103-1 15. REGAN, T. (1983): The case for animal rights. Berkeley: University of California Press. REGAN, T. (1992): Animal rights: what’s in a name? In Animal welfare and !he environment: 49-61. Ryder, R. D. (Ed.). London: Duckworth Press.

130 ZOO CHALLEkGES: PAST. PRESEYT AND FI‘TUKF

RITCHIE, B. W., HARRISON, G . J. & HARRISON, L. R. (Eds) (1994): Avian medicine: principles and applica- tion. Lake Worth, FL: Wingers Publishing, Inc. ROBINSON, M. H. (1998): Enriching the lives of zoo animals, and their welfare: where research can be fundamental. Animal Welfare 7: 151-175. ROLLIN, B. E. (1989): The unheeded cry. Aninial con- sciousness, anirnnl pain and science. Oxford: Oxford University Press.

SAINSBURY, A. W., BENNETT, P. M. B, KIRKWOOD, J . K. (1995): The welfare of free-living wild animals in Europe: harm caused by human activities. Anirnul Welfare 4: 183-206. WEISKRANTZ, L. (1 997): Con.\ciousrte.s.s lost untl found. Oxford: Oxford University Press.

Manuscript submitted 3 August 2000; accepted 27 January 2001

Inr. ZOO Yh. (2003) 3 8 130-141 0 The Zoological Society of London

Characteristics of a world-class zoo or aquarium in the 21st century M. HUTCHINS’ & B. SMITH2 ’ Director1 William Conway Chair and 2Assistant Director, Department of Conservation and Science, American Zoo and Aquarium Association, 8403 Colesville Road, Suite 710, Silver Spring, Maryland 20910, USA

At the start of the 21st century modern zoos and aquariums are expected to contribute to the survival of the species they display, to educate the public, and to maintain the physical and psychological well- being of the animals in their care. For the future, however, zoos and aquariums will have to be extra- ordinary in both quality and accomplishments. In this article the characteristics of a world-class zoo or aquarium are described, ranging from organizational structure and philosophy, and staff recruitment and training, to animal care and husbandry, research, conservation, education and exhibit design. The importance of inter-institutional co-operation, tech- nology, government affairs, marketing and develop- ment, and public relations are also discussed. In the future managers will have to take a more holistic approach to all these characteristics in order to achieve their core mission without losing sight of the primary objectives of the zoo or aquarium.

Key-words: conservation, co-operation, husbandry, organizational structure, recruitment, technology, 2lst century, world class, zoo and aquarium associations

Many authors have examined various trends and speculated about the future of zoological parks and aquariums (e.g. Caras, 1972; Cherfas, 1984; Wheater, 1985; Croke, 1997; Kelly, 1997; Conway,

1999a; Hutchins, this volume). At the start of the 21st century, expectations for modern zoological institutions are high. Among other things, the best modern zoos and aquariums are now expected to contribute to the survival of the species they display, to educate the public and to maintain the physical and psychological well-being of the animals in their care (Shepherdson, 1998; Conway, 1999a; see also articles in Section 1 , this volume). The zoo and aquarium profession has made considerable strides over the past two decades. Time marches on, however, and those institutions considered to be outstanding today could become mediocre tomorrow if they fail to keep up with the accelerating pace of professional and soci- etal change (Ehrenfeld, 1995). The profes- sion is at a critical historical juncture and in the coming century, a ‘world-class’ zoo or aquarium will have to be extraordinary in both quality and accomplishments. Many of the areas in which they will be expected to excel are fairly evident, such