Dept of Biomedical Services, University of Oxford, Oxford, UK and School of Veterinary Medicine and Science, University of Nottingham, UK
Bioculture (Mauritius) Ltd, Riviere des Anguilles, Mauritius
Although the use of wild-born primates in research is banned in some countries, in others it is commonplace. It has been demonstrated that not only do wild-born primates react more strongly to some stressors than those that are captive-born, but they also use inanimate enrichment less. Given our understanding of the consequences of elevated stress for animal welfare, as well as the quality of science, more consideration should be given to the enrichment, and even the use, of wild-born macaques in biomedical research.
It is well-established that environmental enrichment programmes should be well structured, goal defined and targeted at the specific characteristics of the animals for whom improvement in captive conditions, and hence welfare, are desired (Bloomsmith et al. 1991; Young 2003; Honess & Marin 2006b). Important characteristics include the species identity, the age-sex class, and aspects of individual temperament. A characteristic that is not often considered as part of this is the origin or birth context of the animals; specifically whether they were wild- or captive-born.
In Europe, under existing or incoming regulation (e.g. Home Office 1986; EU 2010), the use of wild-born, and even first generation captive-bred, primates is prohibited (except where there is specific justification). Ostensibly, these measures are to protect wild populations through the creation of self-sustaining breeding colonies, and counter the disproportionate stress that captive conditions may impose on naïve animals. However, there are regulatory environments (including the USA) where the housing and scientific use of wild-born animals is permitted. It is therefore important for responsible managers to consider this characteristic as one which may require specific enrichment provision; either in the quantity or quality of the enrichment, or both.
Birth origin and stress
The first question to ask is:
Do wild-born primates react differently to captive environments and routines than captive-born animals? There is evidence from the literature that indeed they do, but not always in the predicted way (Honess & Marin 2006a). For example, a study by Carolyn Crockett and colleagues (2000) found that wild-born female pigtailed macaques (Macaca nemestrina) exhibited more appetite suppression after being moved between rooms than captive-born equivalents. The authors interpret this type of appetite suppression, particularly where it is associated with raised cortisol, to indicate stress. Perhaps more dramatically, other studies have shown that wild-born pigtails also suffer higher mortality associated with translocation (Ha et al. 2000). On the other hand, in rhesus macaques (M. mulatta), wild-born animals have been shown to exhibit less stress-indicative behaviour (self-directed aggression, stereotypies) than captive-born individuals when housed in historically small cages (0.288m3) (Paulk et al. 1977). Of course, lower levels of abnormal behaviour do not in themselves indicate the absence or magnitude of a stress response.
Birth origin and enrichment
So, given that there is evidence that wild-born macaques can react more strongly to some captive management routines, the next question is: Do they react differently to environmental enrichment provided to reduce their stress response?
It has been reported that among older rhesus macaques, those that were wild-born made less use than captive-born of enrichment (wooden sticks, Kong toys, plastic balls) made available to both (Line et al. 1991). Also, in a study comparing enrichment use (Kong toys) between single housed pigtail and long-tailed, or cynomolgus (M. fascicularis) macaques, the fact that the pigtails used the toys more was, at least in part, accounted for by more of them being captive-born, and therefore more familiar with such toys (Crockett et al. 1989).
Birth origin and housing context
Therefore, while there is some evidence both of a heightened stress response and lower use of enrichment in wild-born macaques, it is relatively limited. Nevertheless, what evidence there is might be in line with hypotheses that suggest that animals of such origins might experience significant challenges in adapting to captivity. Having said this, it is likely that the context in which the animal is housed may well be critical in determining the extent of these challenges and their manifestation in the magnitude of the stress response.
Most of the studies cited above involve study subjects that were housed in a socially- and spatially-restricted laboratory environment. Responses may be very different in a breeding facility where animals are housed in species-appropriate, socially-complex groups in expansive caging under ambient tropical conditions. These are the conditions at Bioculture in Mauritius where long-tailed macaques are bred. There is a mixture of wild- and captive-bred animals in this now closed (since 2009) colony and anecdotally there is no meaningful difference in the use of environmental enrichment between them. The extensive range of enrichment (perches, swinging devices, manipulanda and visual barriers, positive reinforcement training and familiarisation to humans) may well mean that there is something provided that appeals to all animals, irrespective of their origin. In the breeding groups with up to forty adults, there is significant social complexity. The housing of primates with compatible conspecifics is perhaps the single most important contribution to their welfare and its beneficial effect is likely to swamp that from inanimate enrichment (Schapiro et al. 1996).
The need for high welfare standards and reduced stress in laboratory animals is well-rehearsed and includes meeting public expectations, addressing the harm:benefit balance and securing the quality of the research model. Where animals have a sustained or significant stress response to captive conditions or research procedures, it not only constitutes a risk to their health but is a source of unwanted variation and confounding variables in research programmes (Poole 1997; Garner 2005), except where these are examining stress itself. Evidence suggests that not only are wild-born macaques likely to react more strongly to stressors but also that they may be more resistant to attempts to ameliorate that response with environmental enrichment, particularly inanimate options. Therefore, for model quality and study design reasons, as well as animal welfare, it makes sense for researchers and procurement staff to obtain captive-born animals for their studies. Such preference will encourage breeding facilities to become self-sustaining with benefits derived from reducing the pressure on threatened native (non-introduced) populations. One of the macaque species most commonly used in research is the long-tailed macaque. This species, that was previously abundant across its natural range in SE Asia, is now reported to be threatened due, in no small part, to uncontrolled removal of animals from the wild for biomedical research (Eudey 2008). Therefore confining primate use to those individuals that are captive-born may have appreciable benefits for animal welfare, the quality of science, and conservation.
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