Honess, P., Andrianjazalahatra, T., Fernandez, L. and Griffiths, M-A.
School of Veterinary Medicine and Science, University of Nottingham, UK.
Bioculture (Mauritius) Ltd, Riviere des Anguilles, Mauritius.

Abstract
The purpose of any well-fashioned environmental enrichment programme should be to meet the behavioural needs of the species concerned. Through meeting these needs, the development of behavioural problems will be avoided and stress and aggression reduced to acceptable levels. The best environmental enrichment programmes ensure that they start from a sound understanding of the ethology of the animal in the wild and make use of safe, available materials and devices in order to release appropriate desired behaviours, eliminate undesired behaviours and enable the animals to exhibit a more natural behavioural repertoire. Inappropriate enrichment, even when safe, is not only a waste of time and money, but may also not achieve the goal of improving animal welfare. In this article, we address some of the issues surrounding the behavioural needs of captive animals and go on to elucidate some of the key aspects of the environmental enrichment strategy at Bioculture (Mauritius) (BCM) designed to balance safety, animal welfare and the practicalities of meeting the appropriate behavioural needs of over 22,000 group-housed long-tailed macaques (Macaca fascicularis).

Introduction
The concept of ethological ‘need’ has rightly received considerable criticism in the past, particularly in the sense that it describes a situation in which an animal deprived of the opportunity to exhibit a behaviour will inevitably suffer as a result (see Dawkins 1983). There are those, however, that make a strong case for the use of such a concept to account for the development of abnormal behaviour, particularly in response to living in captivity in ‘impoverished environments’ (Hughes & Duncan 1988). Applied research in this area of animal welfare has demonstrated that captive animals are not equally motivated to exhibit all behaviours exhibited by wild conspecifics. Dawkins (1983) describes this variation in motivation as indicated by willingness to ‘pay’ a higher price (in terms of time or effort) to gain access to a behavioural opportunity. This reflects, in consumer-economic terms, the ‘elasticity’ of the ‘need’ to exhibit behaviours ranging from the less essential (in captivity), e.g. antipredator behaviour (elastic), to the much more essential, e.g. feeding behaviour (inelastic). Dawkins introduces the important aspect of the evolutionary adaptation of the species, in which the exhibition of certain behaviours improves not only the survival chances of the individual, but also their ability to meet reproductive goals. Complex interactions between the animal’s physical environment, its anatomy, and its ecology are what produce the patterns of individual and species-typical behaviour that we see in wild and, to a lesser extent, captive animals.

Wherever one stands on the debate about the definition and validity of ethological ‘need’, it might be seen as predominantly esoteric and semantic by those trying to design and implement enrichment plans. They may well ask: What does all this mean for designing enrichment programmes? In the case of primates, there is a paucity of the type of elegant consumer-demand studies described by Dawkins (1983), studies designed to elicit the importance of aspects of environmental provision that may be of more, or less, value to the animal. More typically, studies, often beset by confounding factors, have looked at behavioural, physiological or health outcomes for animals maintained without specified provisions in their captive environment or changes in these variables when such provisions are added (Honess & Marin 2006). Despite the theoretical debate and poor availability of demand-based studies, the broad concept of behavioural needs may serve us well in identifying how to tune our housing and husbandry practices for primates. We can, indeed, make a reasonable assumption that to achieve the highest welfare in animals under our care we should work towards:

• Giving the animal a sense of control over its environment (e.g. retreat from humans/ conspecifics: visual barriers);

• Minimising boredom and undesired behaviours;

• Enabling a repertoire and frequency of behaviours that approximates those seen in natural populations in the wild.

An enrichment philosophy led by science and safety
At BCM, we breed highest quality long-tailed macaques (Macaca fascicularis) for biomedical research and employ an ethological and evidence-based approach to their environmental enrichment. The company’s experienced animal care and veterinary staff are guided by postgraduate-qualified primatologists in the species’ appropriate, desirable behaviours and supplied with recommendations on the strategy to achieve the three key aspects listed above. Safety, both for staff and animals, is at the centre of our strategy and all proposed devices and caging modifications are subjected to considerable analysis before cautious in situ testing. Of course, we also pay particular attention to the differing behavioural needs of different age classes: younger animals require more space and structures for play as well as toys to stimulate their psychomotor development. Adults may benefit more from structural enrichment (variety of perching heights, visual barriers, etc.) that enables them to manage social, often dominance-related, priorities.

Social enrichment
For primates, it is clear that the best enrichment comes in the form of appropriate, compatible conspecifics, providing social support that reduces negative responses to many stressors (e.g. Vogt et al. 1981) and improved well-being through appropriate social activity (e.g. allogrooming: Dunbar 2010). Social enrichment is, therefore, the most fundamental component of any macaque enrichment programme (Schapiro et al. 1996). It is also clear that the housing context provides an important factor for enrichment planning. Where animals are already group-housed, the beneficial effects of appropriate, compatible social enrichment may swamp any additional benefit offered by inanimate enrichment (Schapiro et al. 1996). However, if an animal is singly- or pair-housed in a relatively unstimulating environment, as is common at a large number of experimental facilities, then almost any enrichment stands a good chance of, at least in part, occupying the animal’s behavioural void. At BCM, all animals are group-housed; even when temporarily separated for clinical reasons, they are always accompanied by a compatible group-mate. Great care is also taken to maintain social relationships forged in the natal group by keeping weaned animals together when moved into peer groups at 12-15 months of age.

Sensory enrichment
BCM’s animals live outdoors under ambient climatic conditions, with appropriate shelter available from the sun and inclement weather. They have a high level of natural sensory enrichment and stimulation with each group having good views, for example, of other groups, lush tropical vegetation and passing birds. The use of different materials in the cage environment such as wood and plastics, in addition to more traditional metal and concrete, add tactile, textural variety.

Structural enrichment
In an environment such as at BCM, in which so many social and sensory needs are met, much of the enrichment effort focuses on the provision of expansive, functional space and structural complexity. Not only do BCM cages and stocking densities typically exceed the space provision required in most of the world’s testing regulations (EU Directive 2010/63/EU: EU 2010), but great care is taken to ensure that as much of the cage space is as useable as possible. A structural enrichment strategy that is informed by the species’ natural use of space makes better provision for its behavioural needs (Honess In review). Adding height to cages not only allows species-typical vertical retreat when anxious, but also enables the placement of perching sites at different heights to allow species-typical, dominance-related spacing.

Thoughtful planning and use of cage ‘furniture’ not only creates varied travel routes around the cage, which are cognitively stimulating and can discourage excessive route-tracing (Young 2003), but also facilitates species-typical postural behaviour, locomotion (including leaping) and huddling at rest. Examples of other important structural devices that release natural behaviour are cage panels and barrels acting as visual barriers (allowing retreat from the gaze of conspecifics/humans), swinging devices (for coordination and balance) and even, when conditions allow, swimming pools (for exploratory behaviour and play). The affinity of long-tailed macaques for water is indicated by their other name: the crab-eating macaque!

Feeding enrichment
Together with travelling, feeding makes up one of the most substantial daily time allocations of wild macaques (Son 2004). Three key aspects of delivering nutrients in an enriching way include the type of food supplied, and its spatial and temporal distribution. At BCM, in addition to a nutritionally balanced pelleted food, all animals receive a daily allocation of seasonally available, varied, fresh fruit and vegetables which is coarsely chopped and spread across the caging to reduce aggressive competition or monopolisation by dominant individuals. Fresh produce is also hand-fed to all animals as part of our familiarisation programme and they receive preferred food ‘treats’ during positive reinforcement training. While it has been noted that a randomised feeding schedule may be the best at minimizing anticipatory stress (Waitt & Buchanan- Smith 2001), in reality, with such numbers of animals, this is largely impractical and so they are fed at regular times, the next best option to a randomised schedule. Various ways exist for attempting to prolong feeding to approximate the time devoted to this activity in the wild. Concealing food in food puzzles (see ‘Toys” below) or presenting small food items (e.g. seeds) in a forage substrate can result in considerable extensions to time devoted to feeding (Wolfensohn & Honess 2005).

“Toys”
In many cases, enrichment devices marketed for primates have been developed for other species and some, such as KongTM toys, have yet to be shown to have conclusive therapeutic benefits or to hold the monkeys’ attention for long unless refilled with food items or frozen juice (Crockett et al. 1989). Of course, once filled with food/juice, these devices become food puzzles rather than simple toys. Good food puzzles test the dexterity, coordination and cognitive abilities of the animal; but, in order to achieve this, it is necessary to find the correct balance between task difficulty and reward. While many macaques are extractive foragers, the most time- or effort-consuming foraging tasks are reserved for those foods promising the greatest reward (e.g. highest calorie). A very complex puzzle with a ‘cheap’ reward is unlikely to maintain interest once the puzzle element has been solved. Prolonged interest can be achieved by adding high value or novel foods (Holmes et al. 1995).

Commercially available toys and puzzle feeders are typically too costly to provide, even on rotation, for large groups in the numbers necessary to avoid the aggressive competition reported by some authors (Bloomstrand et al. 1986; Maki et al. 1989_ENREF_8). To overcome the issue of cost, toys can be made in house from cheap, readily available and cleanable materials. This approach, which we use at BCM, enables the production of numerous cheap, safe toys whose design is focused on the exploratory and manipulative tendencies of specific age classes, particularly juveniles. Although all BCM animals are extremely high health status, and, like all Mauritian long-tailed macaques, are free from simian herpes B-virus, SRV, SIV, STLV1, SVV care still needs to be taken against other pathogens, and so toys are frequently removed and disinfected.

Conclusion
The cost of enrichment, particularly structural modifications such as increasing cage size and configuration, either in intensive laboratory environments and/or particularly large facilities, can in some instances be daunting and lead to conservatism (e.g. Woolverton et al. 1989). If those controlling budgets for enrichment accept the principle of phased improvements, then at least some of the animals will benefit in the immediate future, rather than waiting for the funds to be available for a major refit. Some excellent resources exist to guide the interested practitioner in designing or refining enrichment strategies for primates: (Bloomsmith et al. 1991; Mellen & MacPhee 2001; Young 2003; Wolfensohn & Honess 2005; Honess & Marin 2006) and include many inexpensive, effective ideas.

At BCM, we believe that we have a well-balanced enrichment strategy that results in animals of exceptionally high welfare status; key to this is our team approach of animal care staff, veterinarians, managers and primatologists. We hope that those with interests/responsibilities in primate welfare will, like the Animal Welfare team at BCM, always strive to learn more about natural primate behaviour. This will enable the development of an enrichment philosophy and strategy grounded in addressing the animals’ extensive range of behavioural needs rather than simply creating an environment that appeals to the human eye, or simply satisfies regulatory minima. Putting the animals’ needs (and reasonable safety) at the centre of our enrichment strategies will not only help meet ethical commitments but will also, through reduced stress, improve research model quality and help convince an often sceptical public that we in the research sector are truly committed to the highest standards of animal welfare.

References
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Volume 10, January 2012

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