Bears and canids have been displayed in zoos since their establishment in the late 18th century, but our association with them is much more ancient (Fisher, 1966; Sanders, 1993; Clutton-Brock, 1999). We have been competitors for food and living space since the Palaeolithic and probably before, and bears and canids have provided fur, food, medicine and entertainment in civilizations, both ancient and modern. Wild canids, first domesticated to assist human hunters and provide protection, now serve many functions as companions created for our indulgences (Clutton-Brock, 1999; Crockford, 2000). Bears and canids are admired for their size, power, hunting prowess and cunning as attributes people have wanted to possess. Even today, human reactions vary from the extremes of the ‘big, bad, wolf’, which must be hunted or eliminated at any cost, to the cuddly pet dog and the teddy bear, and more recently as conservation icons that are romantically invested with powers to transform ecosystems and our experience of wilderness. The current interest in re-wilding depends heavily on the restoration of large predator guilds dominated by predators such as bears and canids (Donlan et al., 2005, 2006; Jeeves, 2006; Nilsen et al., 2007; Manning et al., 2009).
However, it is this perception of power that led to the establishment of an enclosure design that pervaded the zoo world until comparatively recently – the bear pit. This construction offered no opportunity for escape for these powerful predators and also gave opportunities for visitors to entertain themselves, often by feeding the bears unsuitable foods. The provision of a tree or similar climbing apparatus ironically provided among the first forms of environmental enrichment in zoos, although undoubtedly they were also a source of aggression among individuals competing for the best begging pitch (see Berridge & Westell, 1911: facing page 215, fig. 53). As building materials evolved so did the bear pit, such that many city zoos are still littered with tiny concrete prisons, which bring shame on the zoos that still populate them with bears. Interestingly, the bear pit at London Zoo, UK, constructed in c. 1828, was recognized as being inadequate for the bears' welfare (‘a relic of the Middle Ages’) by ZSL's Reorganisation Committee in 1902 and the pit was demolished soon after (Edwards, 1996).
Canids fared little better, often confined to small concrete cages or yards, offering little or no cover and no possibility for normal social dynamics to develop. Optimal management must recognize the complex social systems of many canid species. This is made especially challenging because the basic social unit of many canids is a family group, so assemblages of unrelated individuals are often unstable and associated with aggression. The problem is exacerbated further by a lack of information on social dynamics for many of the lesser-known species. Most would agree that mimicking natural social systems fosters natural behaviours and contributes to well-being, but we are often forced to generalize across species in the absence of data from the field. In addition to the relevance of field research to conservation efforts, data generated from studies of free-ranging populations can inform husbandry and enclosure design.
It is important to distinguish between enclosure design and the care provided by keepers and veterinarians. Poor-quality exhibits do not contribute to animal well-being and they can present a challenge to keepers. However, even in such enclosures, keepers may be able to provide high-quality care in terms of food choices, food presentation, cleanliness, enrichment, etc. The contrast between aesthetics and function should also be recognized because an enclosure that looks beautiful to people may not provide the best environment for the animals living in it.
Thankfully, the situation has improved considerably for most canids in recent years but the requirements for bears are still very much neglected in many zoos. This situation seems paradoxical as bears and canids appear to be among the most popular of zoo animals, but the way they are often displayed and looked after would suggest the opposite. Bears are virtually indestructible despite suffering from a range of viral, bacterial and parasitic diseases (Bourne et al., in press), and they normally live long lives in captivity (Table 1), in comparison with many other species. For example, about one-third of captive Polar bears Ursus maritimus are over the age of 20 years but only 3% of wild bears reach this advanced age (Kitchener, 2004). Recent research is demonstrating that long life is bringing high prevalences of tooth decay and associated abscesses, as well as degenerative joint disease and spondylosis, possibly exacerbated by inactivity (Kitchener, 2004) (Fig. 1). It is unacceptable that dental problems should go untreated; in fact, these should be recorded and dealt with during regular health checks. The monitoring of skeletal problems may be difficult by direct examination but there are effective indirect methods for revealing them. It is critical that more effective protocols be developed to improve the health and well-being of captive bears.
|FEMALE AGE AT|
|American black bear|
|Asian black bear|
The high prevalences of degenerative bone disease in captive bears now provide additional information for zoo managers who are assessing the quality of life of old captive bears (Kitchener, 2004) (Plate 1a–d). Simple behavioural tests or the provision of anti-inflammatories can be used to assess the status of hips and other joints, which may have developed very painful arthroses. More than one zoo manager has thanked me (A.C.K.) for making this information available, which helped them to make what was otherwise proving a very difficult decision as to whether to euthanase an elderly bear or not. Remember, the old sleeping bear may not be content – he may just be in agony if he moves! Canids also live longer in captivity, which means geriatric concerns are similarly inevitable. By euthanasing older bears (and canids) with severe arthroses, enclosure space could be freed up to facilitate the progression of currently stalled captive-breeding programmes.
In the 1990s, there were two important developments in the keeping of bears. Levels of stereotypical behaviours in captive bears confined to concrete pits were rightly regarded as unacceptable by the public and, more importantly, by zoos themselves, although animal welfare organizations undoubtedly played their part in bringing pressure for change. Environmental enrichment, even in small city-zoo bear pits, was developed mainly on the basis of feeding (e.g. scatter feeds, ice blocks), olfactory stimulation (food trails) and the provision of soft substrates, which could allow for digging and other behaviours, thus expanding the potential behavioural repertoire for bears (Ames, 1993a,b).
Canids do not often display stereotypical behaviours to the extent seen in bears but standard care should include enrichment strategies for all captive animals. Ideal enrichment should engage an animal mentally and encourage activity. Studies into a variety of enrichment approaches would be beneficial for all canid species. Such research can also provide insight into social dynamics, sensory perception and innate preferences.
Law & Reid (in press) review the development of and best practice in environmental enrichment for bears from enclosure design to provision of food and materials that elicit particular behaviours. However, it has been discovered that if already learnt, stereotypical behaviours cannot usually be eliminated completely and, thus, we are left with a legacy of bears that appear not to benefit from new techniques and enclosures. It is important that this is interpreted to visitors or misperceptions may continue that bears cannot be kept successfully in zoos.
The second major development was large naturalistic enclosures, which resulted from the use of minimal wire barriers backed up by electric fencing. Although such enclosures have existed for many years, they were expensive to build and unsightly to look at; for example, ZSL Whipsnade Zoo's Brown bear Ursus arctos enclosure, built at the beginning of the 1930s, is surrounded by heavy steel bars. Electric fencing and simpler high-tension wire and mesh barriers are much cheaper, can be used to enclose large areas and do not provide such discouraging visual barriers. The high quality of these new living spaces with numerous opportunities for climbing, digging and natural foraging means that the need for bears to challenge the apparently flimsy barriers is very low, but not completely without risk, especially if any intraspecific aggression overrides an individual's fear of electric fencing.
Very large enclosures have also led to the development of increasing numbers of mixed exhibits. Often these have involved mixes of bears and canids, such as Brown bear and Grey wolf Canis lupus or Arctic fox Alopex (Vulpes) lagopus, but today much more imaginative mixes of species are being tried out (Dorman & Bourne, in press; Law & Reid, in press). For example, at South Lakes Wild Animal Park, UK, a very adventurous but apparently successful mixed exhibit comprises Spectacled bears Tremarctos ornatus, Short-clawed otters Amblonyx cinereus, Brown capuchins Cebus apella, Tapir Tapirus terrestris, Capybara Hydrochaeris hydrochaeris and, just recently, Colombian spider monkeys Ateles fusciceps rufiventris (A. C. Kitchener, pers. obs). By providing sufficient space and structural heterogeneity, species can choose to interact with or avoid each other. Thus, an otherwise dull exhibit of sleeping bears can become a focus of attention with active primates, otters and other species.
The development of new exhibit ideas that take advantage of natural behaviours is also increasing. Encouragement of natural hibernation in Asian black bears Ursus thibetanus began at Glasgow Zoo in the 1980s but a hibernation exhibit has now been developed at Ueno Zoological Gardens (O'Grady et al., 1990; Itoh et al., in press), which provides a fascinating insight into this natural behaviour in bears and other mammals, as well as allowing the bears to exhibit a natural behaviour that may well be important for normal physiological functioning.
Regional captive-breeding programmes, especially Species Survival Plans (SSPs) and European Endangered Species Programmes (EEPs), for canids have undoubtedly been highly successful in establishing viable long-term populations of some species. Maned wolves Chrysocyon brachyurus, Bush dogs Speothus venaticus, African hunting dogs Lycaon pictus and Dholes Cuon alpinus, have all become regulars in European zoos from being exceptional rarities perhaps only 40 years ago. In contrast, Dholes and Bush dogs remain rare in US zoos but African hunting dogs are well represented, and Mexican wolves Canis lupus baileyi and Red wolves Canis rufus have become common as a result of the cooperative recovery programmes between Association of Zoos & Aquariums (AZA) institutions and the US Fish and Wildlife Service. The AZA commitment to Mexican and Red wolves necessitated a reduction in the numbers of generic grey wolves, because space for large canids in zoos is limited. This choice faces small-canid programme managers as well, because some zoos still hold common species, such as Red foxes Vulpes vulpes and Grey foxes Urocyon cinereoargenteus.
Good research is the basis for successful captive husbandry and there are comparative data to draw upon from the many zoos of the world to find out what works and what does not. Maisch's (in press) review of captive husbandry in and reproduction of Dholes has led to significant reductions in pup mortality and the successful establishment of new packs as well as to the initiation of an EEP for this much neglected, increasingly threatened, fast declining but highly attractive species.
Cooperative breeding programmes of the AZA and the European Association of Zoos and Aquaria (EAZA) have been far less successful for bears with notable exceptions, such as the Spectacled bear. In EAZA's Ursid Taxon Advisory Group it was decided that captive populations could not really offer a source population for conservation including reintroduction because there are too many old bears in inadequate housing. Breeding is prevented by and large, mainly by separation of the sexes and contraception, because there is nowhere to house young animals. Euthanasia of old or even very young bears is often not an option both on legal grounds in some countries (e.g. Germany) as well as public unease with euthanasia of such large high-profile animals, which have often been elevated to celebrity status through public naming events or competitions.
Contraception has frequently been used to prevent breeding in carnivores as a less drastic option but it is not without its difficulties (Boutelle & Bertschinger, in press). Hormonal contraception is sometimes irreversible (Chuei et al., 2007) and progestin-based methods can have serious side-effects in carnivores, such as uterine and mammary tumours (Munson et al., 2005), although such side effects are rare in other taxa. New techniques, such as gonadotrophin-releasing hormone agonists, are proving to be much safer. Still, concern has been expressed by zoo staff in some European countries that contraception prevents ♀♀ from exhibiting the normal behaviour patterns associated with mating and parental care. However, in the United States, contraception is primarily recommended to limit and extend inter-birth intervals, not for permanent sterilization. In AZA zoos ♀♀ are usually allowed to reproduce until they are well-represented genetically before contraception is used. An exception would be to contracept animals held in a family group where inbreeding would result if no other actions were taken.
Reintroduction is proving an increasingly important conservation tool for canids, particularly in North America. Red and Mexican wolves, Swift foxes Vulpes velox and Island foxes Urocyon littoralis sspp, have all been the focus of successful attempts using captive breeding to recover species and subspecies, and begin the restoration of wild populations (Asa, in press; Coonan et al., in press; Waters, in press). The Grey wolf has been returned very successfully to Yellowstone National Park, USA, with demonstrable ecological benefits (e.g. Berger et al., 2001), so that large canids are clearly keystone species in their respective ecosystems (Smith & Ferguson, 2005). Waters (in press) highlights the importance of how translocated or captive-bred Swift foxes are treated before release into the wild to the success of the release. This has important lessons not only for reintroductions but also for inter-zoo transfers of individuals, for which there is all too little research but which can be the most stressful event in an animal's life. Most importantly Asa (in press) illustrates that expertise developed by studying animals in captivity can be of direct conservation and welfare benefit to programmes led by government conservation agencies, thus ensuring a higher probability of success. She demonstrates this with two successful conservation programmes involving the Mexican wolf and the Island fox. We can only hope that this expertise and enthusiasm can be directed towards establishing captive-breeding programmes for other seriously threatened canids, such as the Ethiopian wolf Canis simensis, where repeated disease outbreaks are hitting wild populations hard, so that soon it may be too late for this safety net to be established (Sillero-Zubiri & Macdonald, 1997; Macdonald & Sillero-Zubiri, 2004).
Asa's studies of Mexican grey wolves and Island foxes also demonstrate how much can be learned about basic reproductive biology. Although the Mexican wolf project focused on applied conservation (e.g. semen banking), significant effects of inbreeding on semen quality and breeding success were discovered. The monitoring study of Island foxes yielded surprising evidence of induced oestrus and ovulation, a first for a canid. This result, in particular, reminds us how limited our knowledge base is on even very basic parameters such as these. It also emphasizes the importance of data collection from captive animals, because phenomena such as induced ovulation can be difficult if not impossible to document in free-ranging animals.
The development of computer-based tools to ensure that the genetic diversity of populations is maintained by careful management of captive breeding have clearly benefited global breeding programmes for many species but this may not be the situation everywhere. Vanstreels & Pessuti (in press) have analysed the captive Maned wolf population in Brazil. The current status of this population probably reflects typically the situation in North American and European zoos when SSPs and EEPs were first established, with high dependency on wild recruits, high representation of a handful of founders, high cub mortality and poor levels of transfers between zoos. In contrast the well-managed AZA's Maned wolf SSP has improved captive husbandry and developed important supportive links to in situ conservation and education programmes (Songasen & Rodden, in press).
There is an enormous opportunity for established and new breeding programmes to share husbandry and other information, and exchange animals to ensure the highest genetic diversity for all global programmes as well as ensuring that the best field research and conservation programmes are supported. However, bears have not been considered for re-introductions from captive-bred stock, even though translocations have been frequent, although of mixed success, and attempted rehabilitation of orphaned bear cubs has proved very difficult. Huber (in press) reviews this situation and comes to the conclusion that captive bears can only be ambassadors for their wild counterparts, because bear cubs take up to 2 years to learn the bare necessities of life. However, we cannot help thinking that with ingenuity and taking into account appropriate information from in-depth field and behavioural research, a re-introduction protocol could be developed for all bear species if needed. Clearly there is a long way to go and this is an important challenge that we face but we may not have much time as most bear species are becoming increasingly threatened as habitats disappear and demand for bear products increases.
Although big bears and canids are popular exhibit animals and are generally of high conservation importance, smaller bears and canids have received much less attention in recent years. Bauman et al. (in press) review the current situation with regard to small canids in European and North American zoos now that some species, such as Bat-eared fox Otocyon megalotis and Fennec fox Vulpes zerda, are becoming more common. Although few smaller canids are threatened, this situation could change rapidly as habitats continue to be lost and for many species, such as the Small-eared dog Atelocynus microtis or the Tibetan fox Vulpes ferrilata, we have little or no experience of captive husbandry. We should try and learn how to keep these species now, before it is too late, and to ensure that future captive populations are established appropriately from the outset, rather than repeating the mistakes of the past.
Finally, it is important to remind ourselves that taxonomy underpins all conservation. If we do not know what species we are dealing with, if they lack correct scientific names, if the recognized taxa do not reflect the in situ situation but are the products of poor science, then our conservation effort is likely to fail and precious resources will be wasted. For example, the taxonomic status and correct scientific name of the Red wolf is still hotly debated and not resolved, despite considerable resources and effort continuing to be used for its conservation in captivity and in the wild. Kitchener (in press) reviews the current taxonomy of bears and highlights areas that need to be addressed, particularly with respect to geographical variation and the recognition of distinctive populations. Most importantly he makes the case for integrated, comprehensive morphological and molecular studies in order to understand fully the geographical variation within and the differences between species. Zoos can play a very important role in recording accurately and precisely the origins of any wild-caught animals coming in to their collections, providing samples for molecular and other analyses, and taking responsibility for ensuring the preservation of animals that die in their collections so that they can be archived for future research. National Museums Scotland, UK, has collaborated extensively with many UK and some mainland European zoos to preserve as many complete skins and skeletons as possible of bears, canids and other species. However, there is much to do and assistance with the resourcing of this important aspect of zoo animal husbandry is required for long-term development of these new kinds of collections. These collections also allow for many other kinds of studies, including the effects of captivity, such as nutrition, ageing and environmental enrichment, on the development of the skeleton, and can assist in the identification of illegally traded skeletal material and in veterinary investigations.
Although bears and canids have been much neglected compared with other charismatic mammals, there has been a huge resurgence of interest in them both in the wild and captivity. We have gone far beyond merely exhibiting animals for the entertainment of visitors in the menageries of the past. There are enormously exciting developments in captive husbandry, the management of populations, and the synergies that are developing between modern zoos and in situ conservation, and it is the responsibility of all of us to see that this continues to improve through research, innovation and cooperation. However, despite our long association with bears and canids, and centuries of experience managing them in captivity, we still have much to learn. In particular, new naturalistic, possibly mixed-species, exhibits and the provision of species-appropriate environmental enrichment could transform the lot of zoo bears from being merely refugees in concrete ghettos to being at the centre of stunning, dynamic, educational exhibits. Now it is over to you.